Inhibition of serine palmitoyltransferase delays the onset of radiation-induced pulmonary fibrosis through the negative regulation of sphingosine kinase-1 expression

Journal of Lipid Research

Volumn 53, Issue 8, 2012, Pages 1553-1568

  Gorshkova, Irina ^a   Zhou, Tong ^a   Mathew, Biji ^a   Jacobson, Jeffrey R ^a   Takekoshi, Daisuke ^a   Bhattacharya, Palash ^a   Smith, Brett ^a   Aydogan, Bulent ^b   Weichselbaum, Ralph R ^b   Natarajan, Viswanathan ^a   Garcia, Joe G N ^a   Berdyshev, Evgeny V ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Dihydrosphingosine 1 phosphate; Myriocin; Sphingosine 1 phospate

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BIOGENIC AMINE; COLLAGEN; DIHYDROSPHINGOSINE 1 PHOSPHATE; SERINE PALMITOYLTRANSFERASE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 1; THERMOZYMOCIDIN; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; LIPOGENESIS; LUNG FIBROBLAST; LUNG FIBROSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIATION INJURY; UPREGULATION;

ANIMALS; ENZYME INHIBITORS; FATTY ACIDS, MONOUNSATURATED; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MICE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PULMONARY FIBROSIS; RADIATION INJURIES, EXPERIMENTAL; SERINE C-PALMITOYLTRANSFERASE; SIGNAL TRANSDUCTION; SPHINGOSINE; THORAX; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 84863790153     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M026039     Document Type: Article

References (53)

1. Carruthers, S. A., and M. M. Wallington. 2004. Total body irradiation and pneumonitis risk: a review of outcomes. Br. J. Cancer. 90: 2080-2084. (Pubitemid 38869709)
2. Yu, T. K., G. J. Whitman, H. D. Thames, A. U. Buzdar, E. A. Strom, G. H. Perkins, N. R. Schechter, M. D. McNeese, S. W. Kau, E. S. Thomas, et al. 2004. Clinically relevant pneumonitis after sequential paclitaxel-based chemotherapy and radiotherapy in breast cancer patients. J. Natl. Cancer Inst. 96: 1676-1681.
3. Abid, S. H., V. Malhotra, and M. C. Perry. 2001. Radiation-induced and chemotherapy-induced pulmonary injury. Curr. Opin. Oncol. 13: 242-248. (Pubitemid 32578989)
4. Carver, J. R., C. L. Shapiro, A. Ng, L. Jacobs, C. Schwartz, K. S. Virgo, K. L. Hagerty, M. R. Somerfield, and D. J. Vaughn; ASCO Cancer Survivorship Expert Panel. 2007. American Society of Clinical Oncology clinical evidence review on the ongoing care of adult cancer survivors: cardiac and pulmonary late effects. J. Clin. Oncol. 25: 3991-4008. (Pubitemid 47477279)
5. Demedts, M., J. Behr, R. Buhl, U. Costabel, R. Dekhuijzen, H. M. Jansen, W. MacNee, M. Thomeer, B. Wallaert, F. Laurent, et al IFIGENIA Study Group. 2005. High-dose acetylcysteine in idiopathic pulmonary fibrosis. N. Engl. J. Med. 353: 2229-2242. (Pubitemid 41697286)
6. Wynn, T. A. 2011. Integrating mechanisms of pulmonary fibrosis. J. Exp. Med. 208: 1339-1350.
7. Sekine, I., M. Sumi, Y. Ito, H. Nokihara, N. Yamamoto, H. Kunitoh, Y. Ohe, T. Kodama, N. Saijo, and T. Tamura. 2006. Retrospective analysis of steroid therapy for radiation-induced lung injury in lung cancer patients. Radiother. Oncol. 80: 93-97. (Pubitemid 44226433)
8. Duffield, J. S., S. J. Forbes, C. M. Constandinou, S. Clay, M. Partolina, S. Vuthoori, S. Wu, R. Lang, and J. P. Iredale. 2005. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J. Clin. Invest. 115: 56-65. (Pubitemid 40385505)
9. Wilson, M. S., and T. A. Wynn. 2009. Pulmonary fibrosis: pathogenesis, etiology and regulation. Mucosal Immunol. 2: 103-121.
10. Tsoutsou, P. G., and M. I. Koukourakis. 2006. Radiation pneumonitis and fibrosis: mechanisms underlying its pathogenesis and implications for future research. Int. J. Radiat. Oncol. Biol. Phys. 66: 1281-1293.
11. Siwik, D. A., D. L. Chang, and W. S. Colucci. 2000. Interleukin-1β and tumor necrosis factor-α decrease collagen synthesis and increase matrix metalloproteinase activity in cardiac fibroblasts in vitro. Circ. Res. 86: 1259-1265. (Pubitemid 30436667)
12. Mathew, B., J. R. Jacobson, E. Berdyshev, Y. Huang, X. Sun, Y. Zhao, L. M. Gerhold, J. Siegler, C. Evenoski, T. Wang, et al. 2011. Role of sphingolipids in murine radiation-induced lung injury: protection by sphingosine 1-phosphate analogs. FASEB J. 25: 3388-3400.
13. Peng, X., P. M. Hassoun, S. Sammani, B. J. McVerry, M. J. Burne, H. Rabb, D. Pearse, R. M. Tuder, and J. G. Garcia. 2004. Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am. J. Respir. Crit. Care Med. 169: 1245-1251. (Pubitemid 38680403)
14. McVerry, B. J., X. Peng, P. M. Hassoun, S. Sammani, B. A. Simon, and J. G. Garcia. 2004. Sphingosine 1-phosphate reduces vascular leak in murine and canine models of acute lung injury. Am. J. Respir. Crit. Care Med. 170: 987-993. (Pubitemid 39425695)
15. Linn, S. C., H. S. Kim, E. M. Keane, L. M. Andras, E. Wang, and A. H. Merrill, Jr. 2001. Regulation of de novo sphingolipid biosynthesis and the toxic consequences of its disruption. Biochem. Soc. Trans. 29: 831-835. (Pubitemid 33131789)
16. Irizarry, R. A., B. Hobbs, F. Collin, Y. D. Beazer-Barclay, K. J. Antonellis, U. Scherf, and T. P. Speed. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 4: 249-264.
17. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA. 98: 5116-5121. (Pubitemid 32397092)
18. Kanehisa, M., S. Goto, S. Kawashima, Y. Okuno, and M. Hattori. 2004. The kegg resource for deciphering the genome. Nucleic Acids Res. 32: D277-D280. (Pubitemid 38081656)
19. Huang, D. W., Sherman, B. T., and Lempicki, R. A. 2009. Systematic and integrative analysis of large gene lists using david bioinformatics resources. Nat. Protoc. 4: 44-57.
20. Dennis, G., Jr., B. T. Sherman, D. A. Hosack, J. Yang, W. Gao, H. C. Lane, and R. A. Lempicki. 2003. David: database for annotation, visualization, and integrated discovery. Genome Biol. 4: P 3.
21. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
22. Berdyshev, E. V., I. A. Gorshkova, P. Usatyuk, Y. Zhao, B. Saatian, W. Hubbard, and V. Natarajan. 2006. De novo biosynthesis of dihydrosphingosine-1- phosphate by sphingosine kinase 1 in mammalian cells. Cell. Signal. 18: 1779-1792. (Pubitemid 44216131)
23. Vaskovsky, V. E., E. Y. Kostetsky, and I. M. Vasendin. 1975. A universal reagent for phospholipid analysis. J. Chromatogr. 114: 129-141.
24. Berdyshev, E. V., I. A. Gorshkova, J. G. Garcia, V. Natarajan, and W. C. Hubbard. 2005. Quantitative analysis of sphingoid base-1-phosphates as bisacetylated derivatives by liquid chromatography-tandem mass spectrometry. Anal. Biochem. 339: 129-136. (Pubitemid 40342687)
25. Yamaji-Hasegawa, A., A. Takahashi, Y. Tetsuka, Y. Senoh, and T. Kobayashi. 2005. Fungal metabolite sulfamisterin suppresses sphingolipid synthesis through inhibition of serine palmitoyltransferase. Biochemistry. 44: 268-277. (Pubitemid 40095728)
26. Berdyshev, E. V., I. Gorshkova, A. Skobeleva, R. Bittman, X. Lu, S. M. Dudek, T. Mirzapoiazova, J. G. Garcia, and V. Natarajan. 2009. FTY720 inhibits ceramide synthases and up-regulates dihydrosphingosine 1-phosphate formation in human lung endothelial cells. J. Biol. Chem. 284: 5467-5477.
27. Berdyshev, E. V., J. Goya, I. Gorshkova, G. D. Prestwich, H. S. Byun, R. Bittman, and V. Natarajan. 2011. Characterization of sphingosine-1-phosphate lyase activity by electrospray ionization-liquid chromatography/tandem mass spectrometry quantitation of (2E)-hexadecenal. Anal. Biochem. 408: 12-18.
28. Abdollahi, A., M. Li, G. Ping, C. Plathow, S. Domhan, F. Kiessling, L. B. Lee, G. McMahon, H. J. Gröne, K. E. Lipson, et al. 2005. Inhibition of platelet-derived growth factor signaling attenuates pulmonary fibrosis. J. Exp. Med. 201: 925-935. (Pubitemid 40524462)
29. Li, M., A. Abdollahi, H. J. Gröne, K. E. Lipson, C. Belka, and P. E. Huber. 2009. Late treatment with imatinib mesylate ameliorates radiation-induced lung fibrosis in a mouse model. Radiat. Oncol. 4: 66.
30. Kluepfel, D., J. Bagli, H. Baker, M. P. Charest, and A. Kudelski. 1972. Myriocin, a new antifungal antibiotic from Myriococcum albomyces. J. Antibiot. (Tokyo). 25: 109-115.
31. Hojjati, M. R., Z. Li, H. Zhou, S. Tang, C. Huan, E. Ooi, S. Lu, and X. C. Jiang. 2005. Effect of myriocin on plasma sphingolipid metabolism and atherosclerosis in apoE-deficient mice. J. Biol. Chem. 280: 10284-10289. (Pubitemid 40395884)
32. Glaros, E. N., W. S. Kim, C. M. Quinn, W. Jessup, K. A. Rye, and B. Garner. 2008. Reduction of plasma glycosphingolipid levels has no impact on atherosclerosis in apolipoprotein E-null mice. J. Lipid Res. 49: 324-331.
33. Ussher, J. R., T. R. Koves, V. J. Cadete, L. Zhang, J. S. Jaswal, S. J. Swyrd, D. G. Lopaschuk, S. D. Proctor, W. Keung, D. M. Muoio, et al. 2010. Inhibition of de novo ceramide synthesis reverses diet-induced insulin resistance and enhances whole-body oxygen consumption. Diabetes. 59: 2453-2464.
34. Liu, H., M. Sugiura, V. E. Nava, L. C. Edsall, K. Kono, S. Poulton, S. Milstien, T. Kohama, and S. Spiegel. 2000. Molecular cloning and functional characterization of a novel mammalian sphingosine kinase type 2 isoform. J. Biol. Chem. 275: 19513-19520. (Pubitemid 30441543)
35. Bentzen, S. M. 2006. Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nat. Rev. Cancer. 6: 702-713. (Pubitemid 44286002)
36. Yamanaka, M., D. Shegogue, H. Pei, S. Bu, A. Bielawska, J. Bielawski, B. Pettus, Y. A. Hannun, L. Obeid, and M. Trojanowska. 2004. Sphingosine kinase 1 (SPHK1) is induced by transforming growth factor-beta and mediates TIMP-1 up-regulation. J. Biol. Chem. 279: 53994-54001. (Pubitemid 40053131)
37. Kono, Y., T. Nishiuma, Y. Nishimura, Y. Kotani, T. Okada, S. Nakamura, and M. Yokoyama. 2007. Sphingosine kinase 1 regulates differentiation of human and mouse lung fibroblasts mediated by TGF-β1. Am. J. Respir. Cell Mol. Biol. 37: 395-404. (Pubitemid 47502714)
38. Cencetti, F., C. Bernacchioni, P. Nincheri, C. Donati, and P. Bruni. 2010. Transforming growth factor-β1 induces transdifferentiation of myoblasts into myofibroblasts via up-regulation of sphingosine kinase-1/S1P3 axis. Mol. Biol. Cell. 21: 1111-1124.
39. Lin, X., Z. Fuks, and R. Kolesnick. 2000. Ceramide mediates radiation-induced death of endothelium. Crit. Care Med. 28, N87-93.
40. Wang, L., and S. M. Dudek. 2009. Regulation of vascular permeability by sphingosine 1-phosphate. Microvasc. Res. 77: 39-45.
41. Lu, X., C. Sun, W. J. Valentine, E. Shuyu, J. Liu, G. Tigyi, and R. Bittman. 2009. Chiral vinylphosphonate and phosphonate analogues of the immunosuppressive agent FTY720. J. Org. Chem. 74: 3192-3195.
42. Saddoughi, S. A., P. Song, and B. Ogretmen. 2008. Roles of bioactive sphingolipids in cancer biology and therapeutics. Subcell. Biochem. 49: 413-440.
43. Aarthi, J. J., M. A. Darendeliler, and P. N. Pushparaj. 2011. Dissecting the role of the S1P/S1PR axis in health and disease. J. Dent. Res. 90: 841-854.
44. Ohta, E., T. Ohira, K. Matsue, Y. Ikeda, K. Fujii, K. Ohwaki, S. Osuka, Y. Hirabayashi, and M. Sasaki. 2009. Analysis of development of lesions in mice with serine palmitoyltransferase (SPT) deficiency-Sptlc2 conditional knockout mice. Exp. Anim. 58: 515-524.
45. Miyake, Y., Y. Kozutsumi, S. Nakamura, T. Fujita, and T. Kawasaki. 1995. Serine palmitoyltransferase is the primary target of a sphingosine-like immunosuppressant, ISP-1/myriocin. Biochem. Biophys. Res. Commun. 211: 396-403.
46. Shimamura, M., N. Okamoto, Y. Y. Huang, J. Yasuoka, K. Morita, A. Nishiyama, Y. Amano, and T. Mishina. 2006. Induction of promotive rather than suppressive immune responses from a novel NKT cell repertoire Vα19 NKT cell with alpha-mannosyl ceramide analogues consisting of the immunosuppressant ISP-I as the sphingosine unit. Eur. J. Med. Chem. 41: 569-576. (Pubitemid 43766805)
47. Flanders, K. C. 2004. Smad3 as a mediator of the fibrotic response. Int. J. Exp. Pathol. 85: 47-64. (Pubitemid 38703594)
48. Haase, M. G., A. Klawitter, A. Bierhaus, K. K. Yokoyama, M. Kasper, P. Geyer, M. Baumann, and G. B. Baretton. 2008. Inactivation of AP1 proteins by a nuclear serine protease precedes the onset of radiation-induced fibrosing alveolitis. Radiat. Res. 169: 531-542. (Pubitemid 351671519)
49. Travis, E. L., G. Rachakonda, X. Zhou, K. Korhonen, K. R. Sekhar, S. Biswas, and M. L. Freeman. 2011. NRF2 deficiency reduces life span of mice administered thoracic irradiation. Free Radic. Biol. Med. 51: 1175-1183.
50. Anscher, M. S. 2010. Targeting the TGF-beta1 pathway to prevent normal tissue injury after cancer therapy. Oncologist. 15: 350-359.
51. Kim, J. Y., Y. S. Kim, Y. K. Kim, H. J. Park, S. J. Kim, J. H. Kang, Y. P. Wang, H. S. Jang, S. N. Lee, and S. C. Yoon. 2009. The TGF-beta1 dynamics during radiation therapy and its correlation to symptomatic radiation pneumonitis in lung cancer patients. Radiat. Oncol. 4: 59.
52. Johnston, C. J., J. P. Williams, P. Okunieff, and J. N. Finkelstein. 2002. Radiation-induced pulmonary fibrosis: examination of chemokine and chemokine receptor families. Radiat. Res. 157: 256-265. (Pubitemid 34263838)
53. Sun, L., M. C. Louie, K. M. Vannella, C. A. Wilke, A. M. LeVine, B. B. Moore, and T. P. Shanley. 2011. New concepts of IL-10-induced lung fibrosis: fibrocyte recruitment and M2 activation in a CCL2/CCR2 axis. Am. J. Physiol. Lung Cell. Mol. Physiol. 300: L341-L353.