An novel role of sphingosine kinase-1 (SPHK1) in the invasion and metastasis of esophageal carcinoma

Journal of Translational Medicine

Volumn 9, Issue 1, 2011, Pages

  Pan, Jian ^a,b,d   Tao, Yan Fang ^a,b   Zhou, Zhuan ^c,e   Cao, Bang Rong ^e   Wu, Shui Yan ^a   Zhang, Yan Lan ^a   Hu, Shao Yan ^a   Zhao, Wen Li ^a   Wang, Jian ^a   Lou, Guo Liang ^f   Li, Zhen ^f   Feng, Xing ^a   Ni, Jian ^a,b,d  

^a CHILDREN S HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^b PEKING UNION MEDICAL COLLEGE   (China)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^d NANJING MEDICAL UNIVERSITY   (China)

^e CANCER HOSPITAL   (China)

^f SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA; SPHINGOSINE KINASE 1; PHOSPHOTRANSFERASE; SPHINGOSINE KINASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CELL GROWTH; CONTROLLED STUDY; ESOPHAGUS CARCINOMA; FEMALE; GENE; GENE EXPRESSION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; KAPLAN MEIER METHOD; LUNG METASTASIS; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; METASTASIS POTENTIAL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPHK1 GENE; TUMOR GROWTH; TUMOR VOLUME; UPREGULATION; WESTERN BLOTTING; ANIMAL; ENZYME ACTIVATION; ENZYMOLOGY; ESOPHAGUS TUMOR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; ENZYME ACTIVATION; ESOPHAGEAL NEOPLASMS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPHATIC METASTASIS; MICE; NEOPLASM INVASIVENESS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TREATMENT OUTCOME; UP-REGULATION;

EID: 80053173129     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-9-157     Document Type: Article

References (55)

1. Maddams J, Parkin DM, S CD. The cancer burden in the UK in 2007 due to radiotherapy. Int J Cancer
2. Enzinger PC, Mayer RJ. Esophageal cancer. N Engl J Med 2003, 349:2241-2252. 10.1056/NEJMra035010, 14657432.
3. Yoshinaga K, Inoue H, Utsunomiya T, Sonoda H, Masuda T, Mimori K, Tanaka Y, Mori M. N-cadherin is regulated by activin A and associated with tumor aggressiveness in esophageal carcinoma. Clin Cancer Res 2004, 10:5702-5707. 10.1158/1078-0432.CCR-03-0262, 15355896.
4. Ito T, Shimada Y, Hashimoto Y, Kaganoi J, Kan T, Watanabe G, Murakami Y, Imamura M. Involvement of TSLC1 in progression of esophageal squamous cell carcinoma. Cancer Res 2003, 63:6320-6326.
5. Qian H, Lu N, Xue L, Liang X, Zhang X, Fu M, Xie Y, Zhan Q, Liu Z, Lin C. Reduced MTA1 Expression by RNAi Inhibits in Vitro Invasion and Migration of Esophageal Squamous Cell Carcinoma Cell Line. Clin Exp Metastasis 2006,
6. Bao S, Ouyang G, Bai X, Huang Z, Ma C, Liu M, Shao R, Anderson RM, Rich JN, Wang XF. Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 2004, 5:329-339. 10.1016/S1535-6108(04)00081-9, 15093540.
7. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J. Genes that mediate breast cancer metastasis to lung. Nature 2005, 436:518-524. 10.1038/nature03799, 1283098, 16049480.
8. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massague J. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003, 3:537-549. 10.1016/S1535-6108(03)00132-6, 12842083.
9. Gupta GP, Nguyen DX, Chiang AC, Bos PD, Kim JY, Nadal C, Gomis RR, Manova-Todorova K, Massague J. Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 2007, 446:765-770. 10.1038/nature05760, 17429393.
10. Chen XL, Grey JY, Thomas S, Qiu FH, Medford RM, Wasserman MA, Kunsch C. Sphingosine kinase-1 mediates TNF-alpha-induced MCP-1 gene expression in endothelial cells: upregulation by oscillatory flow. Am J Physiol Heart Circ Physiol 2004, 287:H1452-1458. 10.1152/ajpheart.01101.2003, 15191888.
11. Billich A, Bornancin F, Mechtcheriakova D, Natt F, Huesken D, Baumruker T. Basal and induced sphingosine kinase 1 activity in A549 carcinoma cells: function in cell survival and IL-1beta and TNF-alpha induced production of inflammatory mediators. Cell Signal 2005, 17:1203-1217. 10.1016/j.cellsig.2004.12.005, 16038795.
12. Bu S, Yamanaka M, Pei H, Bielawska A, Bielawski J, Hannun YA, Obeid L, Trojanowska M. Dihydrosphingosine 1-phosphate stimulates MMP1 gene expression via activation of ERK1/2-Ets1 pathway in human fibroblasts. Faseb J 2006, 20:184-186.
13. Bonhoure E, Lauret A, Barnes DJ, Martin C, Malavaud B, Kohama T, Melo JV, Cuvillier O. Sphingosine kinase-1 is a downstream regulator of imatinib-induced apoptosis in chronic myeloid leukemia cells. Leukemia 2008, 22:971-979. 10.1038/leu.2008.95, 18401414.
14. Martin C, Lafosse JM, Malavaud B, Cuvillier O. Sphingosine kinase-1 mediates androgen-induced osteoblast cell growth. Biochem Biophys Res Commun 391:669-673.
15. Kapitonov D, Allegood JC, Mitchell C, Hait NC, Almenara JA, Adams JK, Zipkin RE, Dent P, Kordula T, Milstien S, Spiegel S. Targeting sphingosine kinase 1 inhibits Akt signaling, induces apoptosis, and suppresses growth of human glioblastoma cells and xenografts. Cancer Res 2009, 69:6915-6923. 10.1158/0008-5472.CAN-09-0664, 2752891, 19723667.
16. Young N, Pearl DK, Van Brocklyn JR. Sphingosine-1-phosphate regulates glioblastoma cell invasiveness through the urokinase plasminogen activator system and CCN1/Cyr61. Mol Cancer Res 2009, 7:23-32. 10.1158/1541-7786.MCR-08-0061, 2708075, 19147534.
17. Ran Y, Pan J, Hu H, Zhou Z, Sun L, Peng L, Yu L, Sun L, Liu J, Yang Z. A novel role for tissue factor pathway inhibitor-2 in the therapy of human esophageal carcinoma. Hum Gene Ther 2009, 20:41-49. 10.1089/hum.2008.129, 20377370.
18. Pan J, Hu H, Zhou Z, Sun L, Peng L, Yu L, Sun L, Liu J, Yang Z, Ran Y. Tumor-suppressive mir-663 gene induces mitotic catastrophe growth arrest in human gastric cancer cells. Oncol Rep 24:105-112.
19. Jian P, Yanfang T, Zhuan Z, Jian W, Xueming Z, Jian N. MMP28 (epilysin) as a novel promoter of invasion and metastasis in gastric cancer. BMC Cancer 11:200.
20. Jian P, Li ZW, Fang TY, Jian W, Zhuan Z, Mei LX, Yan WS, Jian N. Retinoic acid induces HL-60 cell differentiation via the upregulation of miR-663. J Hematol Oncol 4:20.
21. Guillermet-Guibert J, Davenne L, Pchejetski D, Saint-Laurent N, Brizuela L, Guilbeau-Frugier C, Delisle MB, Cuvillier O, Susini C, Bousquet C. Targeting the sphingolipid metabolism to defeat pancreatic cancer cell resistance to the chemotherapeutic gemcitabine drug. Mol Cancer Ther 2009, 8:809-820. 10.1158/1535-7163.MCT-08-1096, 19372554.
22. Barker HE, Chang J, Cox TR, Lang G, Bird D, Nicolau M, Evans HR, Gartland A, Erler JT. LOXL2-mediated matrix remodeling in metastasis and mammary gland involution. Cancer Res 71:1561-1572.
23. Peng L, Ran YL, Hu H, Yu L, Liu Q, Zhou Z, Sun YM, Sun LC, Pan J, Sun LX, et al. Secreted LOXL2 is a novel therapeutic target that promotes gastric cancer metastasis via the Src/FAK pathway. Carcinogenesis 2009, 30:1660-1669. 10.1093/carcin/bgp178, 19625348.
24. Schietke R, Warnecke C, Wacker I, Schodel J, Mole DR, Campean V, Amann K, Goppelt-Struebe M, Behrens J, Eckardt KU, Wiesener MS. The lysyl oxidases LOX and LOXL2 are necessary and sufficient to repress E-cadherin in hypoxia: insights into cellular transformation processes mediated by HIF-1. J Biol Chem 285:6658-6669.
25. Mochizuki S, Okada Y. ADAMs in cancer cell proliferation and progression. Cancer Sci 2007, 98:621-628. 10.1111/j.1349-7006.2007.00434.x, 17355265.
26. Roy R, Rodig S, Bielenberg D, Zurakowski D, Moses MA. ADAM12 transmembrane and secreted isoforms promote breast tumor growth: a distinct role for ADAM12-S protein in tumor metastasis. J Biol Chem 286:20758-20768.
27. Chakraborty C, Gleeson LM, McKinnon T, Lala PK. Regulation of human trophoblast migration and invasiveness. Can J Physiol Pharmacol 2002, 80:116-124. 10.1139/y02-016, 11934254.
28. Irwin JC, Suen LF, Martina NA, Mark SP, Giudice LC. Role of the IGF system in trophoblast invasion and pre-eclampsia. Hum Reprod 1999, 14(Suppl 2):90-96.
29. Demetriou MC, Kwei KA, Powell MB, Nagle RB, Bowden GT, Cress AE. Integrin A6 Cleavage in Mouse Skin Tumors. Open Cancer J 2008, 2:1-4. 2906811, 20664806.
30. Goplen D, Wang J, Enger PO, Tysnes BB, Terzis AJ, Laerum OD, Bjerkvig R. Protein disulfide isomerase expression is related to the invasive properties of malignant glioma. Cancer Res 2006, 66:9895-9902. 10.1158/0008-5472.CAN-05-4589, 17047051.
31. Hori T, Yamashita Y, Ohira M, Matsumura Y, Muguruma K, Hirakawa K. A novel orthotopic implantation model of human esophageal carcinoma in nude rats: CD44H mediates cancer cell invasion in vitro and in vivo. Int J Cancer 2001, 92:489-496. 10.1002/ijc.1234, 11304682.
32. Le Scolan E, Pchejetski D, Banno Y, Denis N, Mayeux P, Vainchenker W, Levade T, Moreau-Gachelin F. Overexpression of sphingosine kinase 1 is an oncogenic event in erythroleukemic progression. Blood 2005, 106:1808-1816. 10.1182/blood-2004-12-4832, 15890687.
33. Li XD, Miao SY, Wang GL, Yang L, Shu YQ, Yin YM. Amphiregulin and epiregulin expression in colorectal carcinoma and the correlation with clinicopathological characteristics. Onkologie 33:353-358.
34. Orso F, Penna E, Cimino D, Astanina E, Maione F, Valdembri D, Giraudo E, Serini G, Sismondi P, De Bortoli M, Taverna D. AP-2alpha and AP-2gamma regulate tumor progression via specific genetic programs. Faseb J 2008, 22:2702-2714. 10.1096/fj.08-106492, 18443366.
35. Garamszegi N, Garamszegi SP, Scully SP. Matrix metalloproteinase-1 contribution to sarcoma cell invasion. J Cell Mol Med
36. Fidler IJ. The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 2003, 3:453-458. 10.1038/nrc1098, 12778135.
37. Even-Ram S, Yamada KM. Cell migration in 3D matrix. Curr Opin Cell Biol 2005, 17:524-532. 10.1016/j.ceb.2005.08.015, 16112853.
38. Lan T, Shen X, Liu P, Liu W, Xu S, Xie X, Jiang Q, Li W, Huang H. Berberine ameliorates renal injury in diabetic C57BL/6 mice: Involvement of suppression of SphK-S1P signaling pathway. Arch Biochem Biophys 502:112-120.
39. Kohno M, Momoi M, Oo ML, Paik JH, Lee YM, Venkataraman K, Ai Y, Ristimaki AP, Fyrst H, Sano H, et al. Intracellular role for sphingosine kinase 1 in intestinal adenoma cell proliferation. Mol Cell Biol 2006, 26:7211-7223. 10.1128/MCB.02341-05, 1592880, 16980623.
40. Song L, Xiong H, Li M, Liao WT, Wang L, Wu J. Sphingosine kinase-1 Enhances Resistance to Apoptosis through Activation of PI3K/Akt/NF-{kappa}B Pathway in Human Non-small Cell Lung Cancer. Clin Cancer Res
41. Nemoto S, Nakamura M, Osawa Y, Kono S, Itoh Y, Okano Y, Murate T, Hara A, Ueda H, Nozawa Y, Banno Y. Sphingosine kinase isoforms regulate oxaliplatin sensitivity of human colon cancer cells through ceramide accumulation and Akt activation. J Biol Chem 2009, 284:10422-10432. 10.1074/jbc.M900735200, 2667729, 19240026.
42. Sukocheva O, Wang L, Verrier E, Vadas MA, Xia P. Restoring endocrine response in breast cancer cells by inhibition of the sphingosine kinase-1 signaling pathway. Endocrinology 2009, 150:4484-4492. 10.1210/en.2009-0391, 19706837.
43. Sarkar S, Maceyka M, Hait NC, Paugh SW, Sankala H, Milstien S, Spiegel S. Sphingosine kinase 1 is required for migration, proliferation and survival of MCF-7 human breast cancer cells. FEBS Lett 2005, 579:5313-5317. 10.1016/j.febslet.2005.08.055, 16194537.
44. Maceyka M, Alvarez SE, Milstien S, Spiegel S. Filamin A links sphingosine kinase 1 and sphingosine-1-phosphate receptor 1 at lamellipodia to orchestrate cell migration. Mol Cell Biol 2008, 28:5687-5697. 10.1128/MCB.00465-08, 2546923, 18644866.
45. Elloul S, Vaksman O, Stavnes HT, Trope CG, Davidson B, Reich R. Mesenchymal-to-epithelial transition determinants as characteristics of ovarian carcinoma effusions. Clin Exp Metastasis 27:161-172.
46. Visentin B, Vekich JA, Sibbald BJ, Cavalli AL, Moreno KM, Matteo RG, Garland WA, Lu Y, Yu S, Hall HS, et al. Validation of an anti-sphingosine-1-phosphate antibody as a potential therapeutic in reducing growth, invasion, and angiogenesis in multiple tumor lineages. Cancer Cell 2006, 9:225-238. 10.1016/j.ccr.2006.02.023, 16530706.
47. Milstien S, Spiegel S. Targeting sphingosine-1-phosphate: a novel avenue for cancer therapeutics. Cancer Cell 2006, 9:148-150. 10.1016/j.ccr.2006.02.025, 16530698.
48. Hait NC, Oskeritzian CA, Paugh SW, Milstien S, Spiegel S. Sphingosine kinases, sphingosine 1-phosphate, apoptosis and diseases. Biochim Biophys Acta 2006, 1758:2016-2026. 10.1016/j.bbamem.2006.08.007, 16996023.
49. Taha TA, Hannun YA, Obeid LM. Sphingosine kinase: biochemical and cellular regulation and role in disease. J Biochem Mol Biol 2006, 39:113-131. 10.5483/BMBRep.2006.39.2.113, 16584625.
50. Pitson SM, Moretti PA, Zebol JR, Lynn HE, Xia P, Vadas MA, Wattenberg BW. Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. Embo J 2003, 22:5491-5500. 10.1093/emboj/cdg540, 213794, 14532121.
51. Stahelin RV, Hwang JH, Kim JH, Park ZY, Johnson KR, Obeid LM, Cho W. The mechanism of membrane targeting of human sphingosine kinase 1. J Biol Chem 2005, 280:43030-43038. 10.1074/jbc.M507574200, 16243846.
52. Spiegel S, Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 2003, 4:397-407. 10.1038/nrm1103, 12728273.
53. Estrada-Bernal A, Lawler SE, Nowicki MO, Ray Chaudhury A, Van Brocklyn JR. The role of sphingosine kinase-1 in EGFRvIII-regulated growth and survival of glioblastoma cells. J Neurooncol 102:353-366.
54. Shida D, Fang X, Kordula T, Takabe K, Lepine S, Alvarez SE, Milstien S, Spiegel S. Cross-talk between LPA1 and epidermal growth factor receptors mediates up-regulation of sphingosine kinase 1 to promote gastric cancer cell motility and invasion. Cancer Res 2008, 68:6569-6577. 10.1158/0008-5472.CAN-08-0411, 2763580, 18701480.
55. Sukocheva O, Wadham C, Holmes A, Albanese N, Verrier E, Feng F, Bernal A, Derian CK, Ullrich A, Vadas MA, Xia P. Estrogen transactivates EGFR via the sphingosine 1-phosphate receptor Edg-3: the role of sphingosine kinase-1. J Cell Biol 2006, 173:301-310. 10.1083/jcb.200506033, 2063820, 16636149.