Repeated Fractions of X-Radiation to the Breast Fat Pads of Mice Augment Activation of the Autotaxin-Lysophosphatidate-Inflammatory Cycle
Abstract
:1. Introduction
2. Results
2.1. Multiple Fractions of RT Augment Inflammatory Cytokine Secretion from Breast Adipose Tissue
2.2. The Effects of Three Fractions of RT in Tumor-Bearing and Normal Mice
3. Discussion
4. Materials and Methods
4.1. Reagents
4.2. Mouse Model of Breast Cancer with Radiotherapy
4.3. Adipose Tissue Culture and Radiation Exposure
4.4. Multiplex Analysis of Cytokines and Hormones
4.5. Measurement of ATX Activity
4.6. Measurement of Plasma LPA Concentrations
4.7. Quantitative Real-Time PCR (qRT-PCR)
4.8. Immunohistochemistry and Western Blots
4.9. Statistics
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
Abbreviations
References
- Formenti, S.C.; Demaria, S. Systemic effects of local radiotherapy. Lancet Oncol. 2009, 10, 718–726. [Google Scholar] [CrossRef]
- Schaue, D.; Micewicz, E.D.; Ratikan, J.A.; Xie, M.W.; Cheng, G.; McBride, W.H. Radiation and inflammation. Semin. Radiat. Oncol. 2015, 25, 4–10. [Google Scholar] [CrossRef] [PubMed]
- Lumniczky, K.; Candeias, S.M.; Gaipl, U.S.; Frey, B. Editorial: Radiation and the immune system: Current knowledge and future perspectives. Front. Immunol. 2017, 8, 1933. [Google Scholar] [CrossRef] [PubMed]
- Smyth, S.S.; Sciorra, V.A.; Sigal, Y.J.; Pamuklar, Z.; Wang, Z.; Xu, Y.; Prestwich, G.D.; Morris, A.J. Lipid phosphate phosphatases regulate lysophosphatidic acid production and signaling in platelets: Studies using chemical inhibitors of lipid phosphate phosphatase activity. J. Biol. Chem. 2003, 278, 43214–43223. [Google Scholar] [CrossRef] [PubMed]
- Benesch, M.G.; Zhao, Y.Y.; Curtis, J.M.; McMullen, T.P.; Brindley, D.N. Regulation of autotaxin expression and secretion by lysophosphatidate and sphingosine 1-phosphate. J. Lipid Res. 2015, 56, 1134–1144. [Google Scholar] [CrossRef]
- Benesch, M.G.; Ko, Y.M.; Tang, X.; Dewald, J.; Lopez-Campistrous, A.; Zhao, Y.Y.; Lai, R.; Curtis, J.M.; Brindley, D.N.; McMullen, T.P. Autotaxin is an inflammatory mediator and therapeutic target in thyroid cancer. Endocr. Relat. Cancer 2015, 22, 593–607. [Google Scholar] [CrossRef]
- Benesch, M.G.K.; MacIntyre, I.T.K.; McMullen, T.P.W.; Brindley, D.N. Coming of age for autotaxin and lysophosphatidate signaling: Clinical applications for preventing, detecting and targeting tumor-promoting inflammation. Cancers (Basel) 2018, 10, 73. [Google Scholar] [CrossRef]
- Ray, R.; Rai, V. Lysophosphatidic acid converts monocytes into macrophages in both mice and humans. Blood 2017, 129, 1177–1183. [Google Scholar] [CrossRef]
- Benesch, M.G.K.; Yang, Z.; Tang, X.; Meng, G.; Brindley, D.N. Lysophosphatidate signaling: The tumor microenvironments new nemesis. Trends Cancer 2017, 3, 748–752. [Google Scholar] [CrossRef]
- Benesch, M.G.; Ko, Y.M.; McMullen, T.P.; Brindley, D.N. Autotaxin in the crosshairs: Taking aim at cancer and other inflammatory conditions. FEBS Lett. 2014, 588, 2712–2727. [Google Scholar] [CrossRef]
- Magkrioti, C.; Galaris, A.; Kanellopoulou, P.; Stylianaki, E.A.; Kaffe, E.; Aidinis, V. Autotaxin and chronic inflammatory diseases. J. Autoimmun. 2019, 104, 102327. [Google Scholar] [CrossRef] [PubMed]
- Cao, P.; Aoki, Y.; Badri, L.; Walker, N.M.; Manning, C.M.; Lagstein, A.; Fearon, E.R.; Lama, V.N. Autocrine lysophosphatidic acid signaling activates beta-catenin and promotes lung allograft fibrosis. J. Clin. Investg. 2017, 127, 1517–1530. [Google Scholar] [CrossRef] [PubMed]
- Erstad, D.J.; Tager, A.M.; Hoshida, Y.; Fuchs, B.C. The autotaxin-lysophosphatidic acid pathway emerges as a therapeutic target to prevent liver cancer. Mol. Cell. Oncol. 2017, 4, 1311827. [Google Scholar] [CrossRef] [PubMed]
- Farquhar, M.J.; Humphreys, I.S.; Rudge, S.A.; Wilson, G.K.; Bhattacharya, B.; Ciaccia, M.; Hu, K.; Zhang, Q.; Mailly, L.; Reynolds, G.M.; et al. Autotaxin-lysophosphatidic acid receptor signalling regulates hepatitis C virus replication. J. Hepatol. 2017, 66, 919–929. [Google Scholar] [CrossRef] [PubMed]
- Gan, L.; Xue, J.X.; Li, X.; Liu, D.S.; Ge, Y.; Ni, P.Y.; Deng, L.; Lu, Y.; Jiang, W. Blockade of lysophosphatidic acid receptors LPAR1/3 ameliorates lung fibrosis induced by irradiation. Biochem. Biophys. Res. Commun. 2011, 409, 7–13. [Google Scholar] [CrossRef] [PubMed]
- Kaffe, E.; Katsifa, A.; Xylourgidis, N.; Ninou, I.; Zannikou, M.; Harokopos, V.; Foka, P.; Dimitriadis, A.; Evangelou, K.; Moulas, A.N.; et al. Hepatocyte autotaxin expression promotes liver fibrosis and cancer. Hepatology 2017, 65, 1369–1383. [Google Scholar] [CrossRef]
- Oikonomou, N.; Mouratis, M.A.; Tzouvelekis, A.; Kaffe, E.; Valavanis, C.; Vilaras, G.; Karameris, A.; Prestwich, G.D.; Bouros, D.; Aidinis, V. Pulmonary autotaxin expression contributes to the pathogenesis of pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 2012, 47, 566–574. [Google Scholar] [CrossRef]
- Okudaira, S.; Yukiura, H.; Aoki, J. Biological roles of lysophosphatidic acid signaling through its production by autotaxin. Biochimie 2010, 92, 698–706. [Google Scholar] [CrossRef]
- Pradere, J.P.; Klein, J.; Gres, S.; Guigne, C.; Neau, E.; Valet, P.; Calise, D.; Chun, J.; Bascands, J.L.; Saulnier-Blache, J.S.; et al. LPA1 receptor activation promotes renal interstitial fibrosis. J. Am. Soc. Nephrol. 2007, 18, 3110–3118. [Google Scholar] [CrossRef]
- Rancoule, C.; Pradere, J.P.; Gonzalez, J.; Klein, J.; Valet, P.; Bascands, J.L.; Schanstra, J.P.; Saulnier-Blache, J.S. Lysophosphatidic acid-1-receptor targeting agents for fibrosis. Expert Opin. Investig. Drugs 2011, 20, 657–667. [Google Scholar] [CrossRef]
- Sevastou, I.; Kaffe, E.; Mouratis, M.A.; Aidinis, V. Lysoglycerophospholipids in chronic inflammatory disorders: The PLA(2)/LPC and ATX/LPA axes. Biochim. Biophys. Acta 2013, 1831, 42–60. [Google Scholar] [CrossRef] [PubMed]
- Swaney, J.S.; Chapman, C.; Correa, L.D.; Stebbins, K.J.; Bundey, R.A.; Prodanovich, P.C.; Fagan, P.; Baccei, C.S.; Santini, A.M.; Hutchinson, J.H.; et al. A novel, orally active LPA(1) receptor antagonist inhibits lung fibrosis in the mouse bleomycin model. Br. J. Pharmacol. 2010, 160, 1699–1713. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Natarajan, V. Lysophosphatidic acid (LPA) and its receptors: Role in airway inflammation and remodeling. Biochim. Biophys. Acta 2013, 1831, 86–92. [Google Scholar] [CrossRef] [PubMed]
- GLPG1690. Available online: http://www.glpg.com/docs/ view/598b6182b414d-en (accessed on 9 August 2017).
- Palmer, S.M.; Snyder, L.; Todd, J.L.; Soule, B.; Christian, R.; Anstrom, K.; Luo, Y.; Gagnon, R.; Rosen, G. Randomized, double-Blind, placebo-controlled, Phase 2 trial of BMS-986020, a lysophosphatidic acid receptor antagonist for the treatment of idiopathic pulmonary fibrosis. Chest 2018, 154, 1061–1069. [Google Scholar] [CrossRef] [PubMed]
- Dvorak, H.F. Tumors: Wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 1986, 315, 1650–1659. [Google Scholar] [PubMed]
- Schafer, M.; Werner, S. Cancer as an overhealing wound: An old hypothesis revisited. Nat. Rev. Mol. Cell Biol. 2008, 9, 628–638. [Google Scholar] [CrossRef]
- Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef]
- Colotta, F.; Allavena, P.; Sica, A.; Garlanda, C.; Mantovani, A. Cancer-related inflammation, the seventh hallmark of cancer: Links to genetic instability. Carcinogenesis 2009, 30, 1073–1081. [Google Scholar] [CrossRef]
- So, J.; Wang, F.Q.; Navari, J.; Schreher, J.; Fishman, D.A. LPA-induced epithelial ovarian cancer (EOC) in vitro invasion and migration are mediated by VEGF receptor-2 (VEGF-R2). Gynecol. Oncol. 2005, 97, 870–878. [Google Scholar] [CrossRef]
- Brindley, D.N.; Beneasch, M.G.K.; Murph, M.M. Autotaxin: An Enzymatic Augmenter of Malignant Progression Linked to Inflammation; Melanoma; INTECH: Rijeka, Croatia, 2014. [Google Scholar]
- Samadi, N.; Gaetano, C.; Goping, I.S.; Brindley, D.N. Autotaxin protects MCF-7 breast cancer and MDA-MB-435 melanoma cells against Taxol-induced apoptosis. Oncogene 2009, 28, 1028–1039. [Google Scholar] [CrossRef]
- Gaetano, C.G.; Samadi, N.; Tomsig, J.L.; Macdonald, T.L.; Lynch, K.R.; Brindley, D.N. Inhibition of autotaxin production or activity blocks lysophosphatidylcholine-induced migration of human breast cancer and melanoma cells. Mol. Carcinog. 2009, 48, 801–809. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benesch, M.G.; Tang, X.; Maeda, T.; Ohhata, A.; Zhao, Y.Y.; Kok, B.P.; Dewald, J.; Hitt, M.; Curtis, J.M.; McMullen, T.P.; et al. Inhibition of autotaxin delays breast tumor growth and lung metastasis in mice. FASEB J. 2014, 28, 2655–2666. [Google Scholar] [CrossRef] [PubMed]
- Benesch, M.G.; Tang, X.; Dewald, J.; Dong, W.F.; Mackey, J.R.; Hemmings, D.G.; McMullen, T.P.; Brindley, D.N. Tumor-induced inflammation in mammary adipose tissue stimulates a vicious cycle of autotaxin expression and breast cancer progression. FASEB J. 2015, 29, 3990–4000. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Volden, P.A.; Skor, M.N.; Johnson, M.B.; Singh, P.; Patel, F.N.; McClintock, M.K.; Brady, M.J.; Conzen, S.D. Mammary adipose tissue-derived lysophospholipids promote estrogen receptor-negative mammary epithelial cell proliferation. Cancer Prev. Res. (Phila.) 2016, 9, 367–378. [Google Scholar] [CrossRef] [PubMed]
- Schmid, R.; Wolf, K.; Robering, J.W.; Strauss, S.; Strissel, P.L.; Strick, R.; Rubner, M.; Fasching, P.A.; Horch, R.E.; Kremer, A.E.; et al. ADSCs and adipocytes are the main producers in the autotaxin-lysophosphatidic acid axis of breast cancer and healthy mammary tissue in vitro. BMC Cancer 2018, 18, 1273. [Google Scholar] [CrossRef] [Green Version]
- Dusaulcy, R.; Rancoule, C.; Gres, S.; Wanecq, E.; Colom, A.; Guigne, C.; van Meeteren, L.A.; Moolenaar, W.H.; Valet, P.; Saulnier-Blache, J.S. Adipose-specific disruption of autotaxin enhances nutritional fattening and reduces plasma lysophosphatidic acid. J. Lipid Res. 2011, 52, 1247–1255. [Google Scholar] [CrossRef] [Green Version]
- Rancoule, C.; Dusaulcy, R.; Treguer, K.; Gres, S.; Guigne, C.; Quilliot, D.; Valet, P.; Saulnier-Blache, J.S. Depot-specific regulation of autotaxin with obesity in human adipose tissue. J. Physiol. Biochem. 2012, 68, 635–644. [Google Scholar] [CrossRef]
- Lopez-Jaramillo, P.; Gomez-Arbelaez, D.; Lopez-Lopez, J.; Lopez-Lopez, C.; Martinez-Ortega, J.; Gomez-Rodriguez, A.; Triana-Cubillos, S. The role of leptin/adiponectin ratio in metabolic syndrome and diabetes. Horm. Mol. Biol. Clin. Investig. 2014, 18, 37–45. [Google Scholar] [CrossRef] [Green Version]
- Sundaram, S.; Johnson, A.R.; Makowski, L. Obesity, metabolism and the microenvironment: Links to cancer. J. Carcinog. 2013, 12, 19. [Google Scholar]
- De Pergola, G.; Silvestris, F. Obesity as a major risk factor for cancer. J. Obes. 2013, 2013, 291546. [Google Scholar] [CrossRef] [Green Version]
- Liu, S.; Umezu-Goto, M.; Murph, M.; Lu, Y.; Liu, W.; Zhang, F.; Yu, S.; Stephens, L.C.; Cui, X.; Murrow, G.; et al. Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell 2009, 15, 539–550. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Popnikolov, N.K.; Dalwadi, B.H.; Thomas, J.D.; Johannes, G.J.; Imagawa, W.T. Association of autotaxin and lysophosphatidic acid receptor 3 with aggressiveness of human breast carcinoma. Tumour Biol. 2012, 33, 2237–2243. [Google Scholar] [CrossRef] [PubMed]
- St-Coeur, P.D.; Ferguson, D.; Morin, P., Jr.; Touaibia, M. PF-8380 and closely related analogs: Synthesis and structure-activity relationship towards autotaxin inhibition and glioma cell viability. Arch. Pharm. (Weinh.) 2013, 346, 91–97. [Google Scholar] [CrossRef] [PubMed]
- Samadi, N.; Bekele, R.; Capatos, D.; Venkatraman, G.; Sariahmetoglu, M.; Brindley, D.N. Regulation of lysophosphatidate signaling by autotaxin and lipid phosphate phosphatases with respect to tumor progression, angiogenesis, metastasis and chemo-resistance. Biochimie 2011, 93, 61–70. [Google Scholar] [CrossRef]
- Euer, N.; Schwirzke, M.; Evtimova, V.; Burtscher, H.; Jarsch, M.; Tarin, D.; Weidle, U.H. Identification of genes associated with metastasis of mammary carcinoma in metastatic versus non-metastatic cell lines. Anticancer Res. 2002, 22, 733–740. [Google Scholar]
- Castellana, B.; Escuin, D.; Peiro, G.; Garcia-Valdecasas, B.; Vazquez, T.; Pons, C.; Perez-Olabarria, M.; Barnadas, A.; Lerma, E. ASPN and GJB2 are implicated in the mechanisms of invasion of ductal breast carcinomas. J. Cancer 2012, 3, 175–183. [Google Scholar] [CrossRef] [Green Version]
- Vital, A.L.; Tabernero, M.D.; Castrillo, A.; Rebelo, O.; Tao, H.; Gomes, F.; Nieto, A.B.; Resende Oliveira, C.; Lopes, M.C.; Orfao, A. Gene expression profiles of human glioblastomas are associated with both tumor cytogenetics and histopathology. Neuro Oncol. 2010, 12, 991–1003. [Google Scholar] [CrossRef]
- Tang, X.; Benesch, M.G.; Brindley, D.N. Lipid phosphate phosphatases and their roles in mammalian physiology and pathology. J. Lipid Res. 2015, 56, 2048–2060. [Google Scholar] [CrossRef] [Green Version]
- Tang, X.; Benesch, M.G.; Dewald, J.; Zhao, Y.Y.; Patwardhan, N.; Santos, W.L.; Curtis, J.M.; McMullen, T.P.; Brindley, D.N. Lipid phosphate phosphatase-1 expression in cancer cells attenuates tumor growth and metastasis in mice. J. Lipid Res. 2014, 55, 2389–2400. [Google Scholar] [CrossRef] [Green Version]
- Tang, X.; Wang, X.; Zhao, Y.Y.; Curtis, J.M.; Brindley, D.N. Doxycycline attenuates breast cancer related inflammation by decreasing plasma lysophosphatidate concentrations and inhibiting NF-kappaB activation. Mol. Cancer 2017, 16, 36. [Google Scholar] [CrossRef] [Green Version]
- Tang, X.; McMullen, T.P.; Brindley, D.N. Increasing the low lipid phosphate phosphatase 1 activity in breast cancer cells decreases transcription by AP-1 and expressions of matrix metalloproteinases and cylin D1/D3. Theranostics 2019, 9, 6129–6142. [Google Scholar] [CrossRef] [PubMed]
- Bekele, R.T.; Venkatraman, G.; Liu, R.Z.; Tang, X.; Mi, S.; Benesch, M.G.; Mackey, J.R.; Godbout, R.; Curtis, J.M.; McMullen, T.P.; et al. Oxidative stress contributes to the tamoxifen-induced killing of breast cancer cells: Implications for tamoxifen therapy and resistance. Sci. Rep. 2016, 6, 21164. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Venkatraman, G.; Benesch, M.G.; Tang, X.; Dewald, J.; McMullen, T.P.; Brindley, D.N. Lysophosphatidate signaling stabilizes Nrf2 and increases the expression of genes involved in drug resistance and oxidative stress responses: Implications for cancer treatment. FASEB J. 2015, 29, 772–785. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schaue, D.; Kachikwu, E.L.; McBride, W.H. Cytokines in radiobiological responses: A review. Radiat. Res. 2012, 178, 505–523. [Google Scholar] [CrossRef]
- Bower, J.E.; Ganz, P.A.; Tao, M.L.; Hu, W.; Belin, T.R.; Sepah, S.; Cole, S.; Aziz, N. Inflammatory biomarkers and fatigue during radiation therapy for breast and prostate cancer. Clin. Cancer Res. 2009, 15, 5534–5540. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Meng, G.; Tang, X.; Yang, Z.; Benesch, M.G.K.; Marshall, A.; Murray, D.; Hemmings, D.G.; Wuest, F.; McMullen, T.P.W.; Brindley, D.N. Implications for breast cancer treatment from increased autotaxin production in adipose tissue after radiotherapy. FASEB J. 2017, 31, 4064–4077. [Google Scholar] [CrossRef] [Green Version]
- Balogh, A.; Shimizu, Y.; Lee, S.C.; Norman, D.D.; Gangwar, R.; Bavaria, M.; Moon, C.; Shukla, P.; Rao, R.; Ray, R.; et al. The autotaxin-LPA2 GPCR axis is modulated by gamma-irradiation and facilitates DNA damage repair. Cell Signal. 2015, 27, 1751–1762. [Google Scholar] [CrossRef] [Green Version]
- Tang, X.; Wuest, M.; Benesch, M.; Dufour, J.; Zhao, Y.; Curtis, J.; Monjardet, A.; Heckmann, B.; Murray, D.; Wuest, F.; et al. Inhibition of ATX with GLPG1690 increases the efficacy of radiotherapy and chemotherapy in a mouse model of breast cancer. Mol. Cancer Ther. 2019. [Google Scholar] [CrossRef] [Green Version]
- Meng, G.; Tang, X.; Yang, Z.; Zhao, Y.; Curtis, J.M.; McMullen, T.P.W.; Brindley, D.N. Dexamethasone decreases the autotaxin-lysophosphatidate-inflammatory axis in adipose tissue: Implications for the metabolic syndrome and breast cancer. FASEB J. 2019, 33, 1899–1910. [Google Scholar] [CrossRef] [Green Version]
- Ma, Q. Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 2013, 53, 401–426. [Google Scholar] [CrossRef] [Green Version]
- Jayakumar, S.; Pal, D.; Sandur, S.K. Nrf2 facilitates repair of radiation induced DNA damage through homologous recombination repair pathway in a ROS independent manner in cancer cells. Mutat. Res. 2015, 779, 33–45. [Google Scholar] [CrossRef] [PubMed]
- Lee, S.; Lim, M.J.; Kim, M.H.; Yu, C.H.; Yun, Y.S.; Ahn, J.; Song, J.Y. An effective strategy for increasing the radiosensitivity of Human lung Cancer cells by blocking Nrf2-dependent antioxidant responses. Free Radic. Biol. Med. 2012, 53, 807–816. [Google Scholar] [CrossRef] [PubMed]
- Murray, D.; Mirzayans, R.; McBride, W.H. Defenses against pro-oxidant forces - Maintenance of cellular and genomic integrity and longevity. Radiat. Res. 2018, 190, 331–349. [Google Scholar] [CrossRef] [PubMed]
- Lau, A.; Tian, W.; Whitman, S.A.; Zhang, D.D. The predicted molecular weight of Nrf2: It is what it is not. Antioxid. Redox Signal. 2013, 18, 91–93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dalamaga, M.; Diakopoulos, K.N.; Mantzoros, C.S. The role of adiponectin in cancer: A review of current evidence. Endocr. Rev. 2012, 33, 547–594. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Davies, L.C.; Jenkins, S.J.; Allen, J.E.; Taylor, P.R. Tissue-resident macrophages. Nat. Immunol. 2013, 14, 986–995. [Google Scholar] [CrossRef]
- Brindley, D.N.; Lin, F.T.; Tigyi, G.J. Role of the autotaxin-lysophosphatidate axis in cancer resistance to chemotherapy and radiotherapy. Biochim. Biophys. Acta 2013, 1831, 74–85. [Google Scholar] [CrossRef] [Green Version]
- E, S.; Lai, Y.J.; Tsukahara, R.; Chen, C.S.; Fujiwara, Y.; Yue, J.; Yu, J.H.; Guo, H.; Kihara, A.; Tigyi, G.; et al. Lysophosphatidic acid 2 receptor-mediated supramolecular complex formation regulates its antiapoptotic effect. J. Biol. Chem. 2009, 284, 14558–14571. [Google Scholar] [CrossRef] [Green Version]
- Lin, F.T.; Lai, Y.J.; Makarova, N.; Tigyi, G.; Lin, W.C. The lysophosphatidic acid 2 receptor mediates down-regulation of Siva-1 to promote cell survival. J. Biol. Chem. 2007, 282, 37759–37769. [Google Scholar] [CrossRef] [Green Version]
- Hait, N.C.; Maiti, A. The role of sphingosine-1-phosphate and ceramide-1-phosphate in inflammation and cancer. Mediat. Inflamm. 2017, 2017, 4806541. [Google Scholar] [CrossRef]
- Espaillat, M.P.; Kew, R.R.; Obeid, L.M. Sphingolipids in neutrophil function and inflammatory responses: Mechanisms and implications for intestinal immunity and inflammation in ulcerative colitis. Adv. Biol. Regul. 2017, 63, 140–155. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nagahashi, M.; Yamada, A.; Katsuta, E.; Aoyagi, T.; Huang, W.C.; Terracina, K.P.; Hait, N.C.; Allegood, J.C.; Tsuchida, J.; Yuza, K.; et al. Targeting the SphK1/S1P/S1PR1 axis that links obesity, chronic inflammation, and breast cancer metastasis. Cancer Res. 2018, 78, 1713–1725. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Blaho, V.A.; Hla, T. An update on the biology of sphingosine 1-phosphate receptors. J. Lipid Res. 2014, 55, 1596–1608. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stern, J.H.; Rutkowski, J.M.; Scherer, P.E. Adiponectin, leptin, and fatty acids in the maintenance of metabolic homeostasis through adipose tissue crosstalk. Cell Metab. 2016, 23, 770–784. [Google Scholar] [CrossRef] [PubMed]
- Desai, S.; Kumar, A.; Laskar, S.; Pandey, B.N. Cytokine profile of conditioned medium from human tumor cell lines after acute and fractionated doses of gamma radiation and its effect on survival of bystander tumor cells. Cytokine 2013, 61, 54–62. [Google Scholar] [CrossRef] [PubMed]
- Di Maggio, F.M.; Minafra, L.; Forte, G.I.; Cammarata, F.P.; Lio, D.; Messa, C.; Gilardi, M.C.; Bravatà, V. Portrait of inflammatory response to ionizing radiation treatment. J. Inflamm. (Lond.) 2015, 12, 14. [Google Scholar] [CrossRef] [Green Version]
- Multhoff, G.; Radons, J. Radiation, inflammation, and immune responses in cancer. Front. Oncol 2012, 2, 58. [Google Scholar] [CrossRef] [Green Version]
- Wara, W.M. Immunosuppression associated with radiation therapy. Int. J. Radiat. Oncol. Biol. Phys. 1977, 2, 593–596. [Google Scholar] [CrossRef]
- Wu, C.T.; Chen, M.F.; Chen, W.C.; Hsieh, C.C. The role of IL-6 in the radiation response of prostate cancer. Radiat. Oncol. 2013, 8, 159. [Google Scholar] [CrossRef] [Green Version]
- Paquette, B.; Therriault, H.; Wagner, J.R. Role of interleukin-1β in radiation-enhancement of MDA-MB-231 breast cancer cell invasion. Radiat. Res. 2013, 180, 292–298. [Google Scholar] [CrossRef]
- Centurione, L.; Aiello, F.B. DNA repair and cytokines: TGF-β, IL-6, and thrombopoietin as different biomarkers of radioresistance. Front. Oncol. 2016, 6, 175. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, H.; Yue, J.; Jiang, Z.; Zhou, R.; Xie, R.; Xu, Y.; Wu, S. CAF-secreted CXCL1 conferred radioresistance by regulating DNA damage response in a ROS-dependent manner in esophageal squamous cell carcinoma. Cell Death Dis. 2017, 8, 27900. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, S.; Lu, H.; Bai, Y. Nrf2 in cancers: A double-edged sword. Cancer Med. 2019, 8, 2252–2267. [Google Scholar] [CrossRef] [PubMed]
- Cloer, E.W.; Goldfarb, D.; Schrank, T.P.; Weissman, B.E.; Major, M.B. NRF2 activation in cancer: From DNA to protein. Cancer Res. 2019, 79, 889–898. [Google Scholar] [CrossRef] [Green Version]
- Li, B.; Wang, X.; Rasheed, N.; Hu, Y.; Boast, S.; Ishii, T.; Nakayama, K.; Nakayama, K.I.; Goff, S.P. Distinct roles of c-Abl and Atm in oxidative stress response are mediated by protein kinase C delta. Genes Dev. 2004, 18, 1824–1837. [Google Scholar] [CrossRef] [Green Version]
- Chen, W.; Sun, Z.; Wang, X.J.; Jiang, T.; Huang, Z.; Fang, D.; Zhang, D.D. Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxidant response. Mol. Cell 2009, 34, 663–673. [Google Scholar] [CrossRef] [Green Version]
- Brown, J.M.; Attardi, L.D. The role of apoptosis in cancer development and treatment response. Nat. Rev. Cancer 2005, 5, 231–237. [Google Scholar] [CrossRef]
- Khadrawy, O.; Gebremedhn, S.; Salilew-Wondim, D.; Taqi, M.O.; Neuhoff, C.; Tholen, E.; Hoelker, M.; Schellander, K.; Tesfaye, D. Endogenous and exogenous modulation of Nrf2 mediated oxidative stress response in bovine granulosa cells: Potential implication for ovarian function. Int. J. Mol. Sci. 2019, 20, 1635. [Google Scholar] [CrossRef] [Green Version]
- Kwak, M.K.; Itoh, K.; Yamamoto, M.; Kensler, T.W. Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: Role of antioxidant response element-like sequences in the nrf2 promoter. Mol. Cell. Biol. 2002, 22, 2883–2892. [Google Scholar] [CrossRef] [Green Version]
- Schleicher, S.M.; Thotala, D.K.; Linkous, A.G.; Hu, R.; Leahy, K.M.; Yazlovitskaya, E.M.; Hallahan, D.E. Autotaxin and LPA receptors represent potential molecular targets for the radiosensitization of murine glioma through effects on tumor vasculature. PLoS ONE 2011, 6, e22182. [Google Scholar] [CrossRef] [Green Version]
- Bhave, S.R.; Dadey, D.Y.; Karvas, R.M.; Ferraro, D.J.; Kotipatruni, R.P.; Jaboin, J.J.; Hallahan, A.N.; Dewees, T.A.; Linkous, A.G.; Hallahan, D.E.; et al. Autotaxin inhibition with PF-8380 enhances the radiosensitivity of human and murine glioblastoma cell lines. Front. Oncol. 2013, 3, 00236. [Google Scholar] [CrossRef] [PubMed] [Green Version]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Meng, G.; Wuest, M.; Tang, X.; Dufour, J.; Zhao, Y.; Curtis, J.M.; McMullen, T.P.W.; Murray, D.; Wuest, F.; Brindley, D.N. Repeated Fractions of X-Radiation to the Breast Fat Pads of Mice Augment Activation of the Autotaxin-Lysophosphatidate-Inflammatory Cycle. Cancers 2019, 11, 1816. https://doi.org/10.3390/cancers11111816
Meng G, Wuest M, Tang X, Dufour J, Zhao Y, Curtis JM, McMullen TPW, Murray D, Wuest F, Brindley DN. Repeated Fractions of X-Radiation to the Breast Fat Pads of Mice Augment Activation of the Autotaxin-Lysophosphatidate-Inflammatory Cycle. Cancers. 2019; 11(11):1816. https://doi.org/10.3390/cancers11111816
Chicago/Turabian StyleMeng, Guanmin, Melinda Wuest, Xiaoyun Tang, Jennifer Dufour, YuanYuan Zhao, Jonathan M. Curtis, Todd P. W. McMullen, David Murray, Frank Wuest, and David N. Brindley. 2019. "Repeated Fractions of X-Radiation to the Breast Fat Pads of Mice Augment Activation of the Autotaxin-Lysophosphatidate-Inflammatory Cycle" Cancers 11, no. 11: 1816. https://doi.org/10.3390/cancers11111816