Regulation of hematogenous tumor metastasis by acid sphingomyelinase

EMBO Molecular Medicine

Volumn 7, Issue 6, 2015, Pages 714-734

  Carpinteiro, Alexander ^a,b   Becker, Katrin Anne ^a   Japtok, Lukasz ^c   Hessler, Gabriele ^a   Keitsch, Simone ^a   Požgajovà, Miroslava ^d   Schmid, Kurt W ^b   Adams, Constantin ^a   Müller, Stefan ^b   Kleuser, Burkhard ^c   Edwards, Michael J ^e   Grassmé, Heike ^a   Helfrich, Iris ^b   Gulbins, Erich ^a,e  

^a UNIVERSITY OF ESSEN MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

^c UNIVERSITY OF POTSDAM   (Germany)

^d SLOVAK UNIVERSITY OF AGRICULTURE IN NITRA   (Slovakia)

^e UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Acid sphingomyelinase; Ceramide; Integrins; Platelets; Tumor metastasis

Indexed keywords

BETA1 INTEGRIN; INTEGRIN; SPHINGOMYELIN PHOSPHODIESTERASE; VERY LATE ACTIVATION ANTIGEN 5; ASMASE, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL ADHESION; CELL INTERACTION; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG METASTASIS; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; DEFICIENCY; KNOCKOUT MOUSE; MELANOMA; METABOLISM; METASTASIS; PATHOPHYSIOLOGY; SECONDARY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; MELANOMA; MICE; MICE, KNOCKOUT; NEOPLASM METASTASIS; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 84930180779     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201404571     Document Type: Article

References (63)

1. Bauer J, Huy C, Brenmoehl J, Obermeier F, Bock J (2009) Matrix metalloproteinase-1 expression induced by IL-1beta requires acid sphingomyelinase. FEBS Lett 583: 915-920
2. Bock J, Gulbins E (2003) The transmembranous domain of CD40 determines CD40 partitioning into lipid rafts. FEBS Lett 534: 169-174
3. Bray D, Levin MD, Morton-Firth CJ (1998) Receptor clustering as a cellular mechanism to control sensitivity. Nature 393: 85-88
4. Bretti S, Neri P, Lozzi L, Rustici M, Comoglio P, Giancotti F, Tarone G (1989) Inhibition of experimental metastasis of murine fibrosarcoma cells by oligopeptide analogues to the fibronectin cell-binding site. Int J Cancer 43: 102-106
5. Crissman JD, Hatfield JS, Menter DG, Sloane B, Honn KV (1988) Morphological study of the interaction of intravascular tumor cells with endothelial cells and subendothelial matrix. Cancer Res 48: 4065-4072
6. Dhami R, He X, Gordon RE, Schuchman EH (2001) Analysis of the lung pathology and alveolar macrophage function in the acid sphingomyelinase-deficient mouse model of Niemann-Pick disease. Lab Invest 81: 987-999
7. Dhami R, Schuchman EH (2004) Mannose 6-phospohate receptor-mediated uptake is defective in acid sphingomyleinase-deficient macrophages. J Biol Chem 279: 1526-1532
8. Dumitru CA, Gulbins E (2006) TRAIL activates acid sphingomyelinase via a redox mechanism and releases ceramide to trigger apoptosis. Oncogene 25: 5612-5625
9. Fayyaz S, Henkel J, Japtok L, Krämer S, Damm G, Seehofer D, Püschel GP, Kleuser B (2014) Involvement of sphingosine 1-phosphate in palmitate-induced resistance of hepatocytes via the S1P2 receptor subtype. Diabetologia 57: 373-382
10. Fidler IJ (1975) Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res 35: 218-224
11. Gasic GJ, Gasic TB, Stewart CC (1968) Antimetastatic effects associated with platelet reduction. Proc Natl Acad Sci USA 61: 46-52
12. Gasic GJ, Gasic TB, Galanti N, Johnson T, Murphy S (1973) Platelet-tumor-cell interactions in mice. The role of platelets in the spread of malignant disease. Int J Cancer 11: 704-718
13. Gehlsen KR, Davis GE, Sriramarao P (1992) Integrin expression in human melanoma cells with differing invasive and metastatic properties. Clin Exp Metastasis 10: 111-120
14. Giancotti FG, Ruoslahti E (1999) Integrin signaling. Science 285: 1028-1032
15. Grassmé H, Jekle A, Riehle A, Schwarz H, Berger J, Sandhoff K, Kolesnick R, Gulbins E (2001) CD95 signaling via ceramide-rich membrane rafts. J Biol Chem 276: 20589-20596
16. Grassmé H, Jendrossek V, Bock J, Riehle A, Gulbins E (2002) Ceramide-rich membrane rafts mediate CD40 clustering. J Immunol 168: 298-307
17. Grossi IM, Hatfield JS, Fitzgerald LA, Newcombe M, Taylor JD, Honn KV (1998) Role of tumor cell glycoproteins immunologically related to glycoproteins Ib and IIb/IIIa in tumor cell-platelet and tumor cell-matrix interactions. FASEB J 2: 2385-2395
18. Gulbins E, Palmada M, Reichel M, Lüth A, Böhmer C, Amato D, Müller CP, Tischbirek CH, Groemer TW, Tabatabai G et al (2013) Acid sphingomyelinase/ceramide system mediates effects of antidepressant drugs. Nat Med 19: 934-938
19. Hannun YA, Obeid LM (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9: 139-150
20. He Q, Riley RT, Sharma RP (2005) Myriocin prevents fumonisin B1-induced sphingoid base accumulation in mice liver without ameliorating hepatotoxicity. Food Chem Toxicol 43: 969-979
21. Helfrich I, Scheffrahn I, Bartling S, Weis J, von Felbert V, Middleton M, Kato M, Ergün S, Augustin HG, Schadendorf D (2010) Resistance to antiangiogenic therapy is directed by vascular phenotype, vessel stabilization, and maturation in malignant melanoma. J Exp Med 207: 491-503
22. Herz J, Pardo J, Kashkar H, Schramm M, Kuzmenkina E, Bos E, Wiegmann K, Wallich R, Peters PJ, Herzig S et al (2009) Acid sphingomyelinase is a key regulator of cytotoxic granule secretion by primary T lymphocytes. Nat Immunol 10: 761-768
23. Honn KV, Tang DG, Crissman JD (1992) Platelets and cancer metastasis: a causal relationship? Cancer Metastasis Rev 11: 325-351
24. Humphries MJ, Olden K, Yamada KM (1986) A synthetic peptide from fibronectin inhibits experimental metastasis of murine melanoma cells. Science 233: 467-470
25. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687
26. Ikegami M, Dhami R, Schuchman EH (2003) Alveolar lipoproteinosis in an acid sphingomyelinase-deficient mouse model of Niemann-Pick disease. Am J Physiol Lung Cell Mol Physiol 284: L518-L525
27. Ishibashi Y, Nakasone T, Kiyohara M, Horibata Y, Sakaguchi K, Hijikata A, Ichinose S, Omori A, Yasui Y, Imamura A et al (2007) A novel endoglycoceramidase hydrolyzes oligogalactosylceramides to produce galactooligosaccharides and ceramides. J Biol Chem 282: 11386-11396
28. Jin S, Yi F, Zhang F, Poklis JL, Li PL (2008) Lysosomal targeting and trafficking of acid sphingomyelinase to lipid raft platforms in coronary endothelial cells. Arterioscler Thromb Vasc Biol 28: 2056-2062
29. Juliano RL, Varner JA (1993) Adhesion molecules in cancer: the role of integrins. Curr Opin Cell Biol 5: 812-818
30. Kato M, Takahashi M, Akhand AA, Liu W, Dai Y, Shimizu S, Iwamoto T, Suzuki H, Nakashima I (1998) Transgenic mouse model for skin malignant melanoma. Oncogene 17: 1885-1888
31. Kim YJ, Borsig L, Varki NM, Varki A (1998) P-selectin deficiency attenuates tumor growth and metastasis. Proc Natl Acad Sci USA 95: 9325-9330
32. Kolesnick RN, Goni FM, Alonso A (2000) Compartmentalization of ceramide signaling: physical foundations and biological effects. J Cell Physiol 184: 285-300
33. Kolzer M, Werth N, Sandhoff K (2004) Interactions of acid sphingomyelinase and lipid bilayers in the presence of the tricyclic antidepressant desipramine. FEBS Lett 559: 96-98
34. Kramer RH, McDonald KA, Crowley E, Ramos DM, Damsky CH (1989) Melanoma cell adhesion to basement membrane mediated by integrin-related complexes. Cancer Res 49: 393-402
35. Liotta LA (1992) Cancer cell invasion and metastasis. Sci Am 266: 54-59
36. Lozano J, Morales A, Cremesti A, Fuks Z, Tilly JL, Schuchman E, Gulbins E, Kolesnick R (2001) Niemann-Pick Disease versus acid sphingomyelinase deficiency. Cell Death Differ 8: 100-1033
37. Mehlen P, Puisieux A (2006) Metastasis: a question of life or death. Nat Rev Cancer 6: 449-458
38. Menter DG, Hatfield JS, Harkins C, Sloane BF, Taylor JD, Crissman JD, Honn KV (1987) Tumor cell-platelet interactions in vitro and their relationship to in vivo arrest of hematogenously circulating tumor cells. Clin Exp Metastasis 5: 65-78
39. Nieswandt B, Hafner M, Echtenacher B, Mannel DN (1999) Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res 59: 1295-1300
40. Nip J, Shibata H, Loskutoff DJ, Cheresh DA, Brodt P (1992) Human melanoma cells derived from lymphatic metastases use integrin alpha v beta 3 to adhere to lymph node vitronectin. J Clin Invest 90: 1406-1413
41. Okino N, He X, Gatt S, Sandhoff K, Ito M, Schuchman EH (2003) The reverse activity of human acid ceramidase. J Biol Chem 278: 29948-29953
42. Oninla VO, Breiden B, Babalola JO, Sandhoff K (2014) Acid sphingomyelinase activity is regulated by membrane lipids and facilitates cholesterol transfer by NPC. J Lipid Res 55: 2606-2619
43. Osawa Y, Suetsugu A, Matsushima-Nishiwaki R, Yasuda I, Saibara T, Moriwaki H, Seishima M, Kozawa O (2013) Liver acid sphingomyelinase inhibits growth of metastatic colon cancer. J Clin Invest 123: 834-843
44. Paschall AV, Zimmerman MA, Torres CM, Yang D, Chen MR, Li X, Bieberich E, Bai A, Bielawski J, Bielawska A et al (2014) Ceramide targets xIAP and cIAP1 to sensitize metastatic colon and breast cancer cells to apoptosis induction to suppress tumor progression. BMC Cancer 14: 24
45. Petersen NH, Olsen OD, Groth-Pedersen L, Ellegaard AM, Bilgin M, Redmer S, Ostenfeld MS, Ulanet D, Dovmark TH, Lønborg A et al (2013) Transformation-associated changes in sphingolipid metabolism sensitize cells to lysosomal cell death induced by inhibitors of acid sphingomyelinase. Cancer Cell 24: 379-393
46. Pewzner-Jung Y, Tavakoli TS, Grassmé H, Becker KA, Japtok L, Steinmann J, Joseph T, Lang S, Tuemmler B, Schuchman EH et al (2014) Sphingoid long chain bases prevent lung infection by Pseudomonas aeruginosa. EMBO Mol Med 6: 1205-1211
47. Pignatelli M, Liu D, Nasim MM, Stamp GW, Hirano S, Takeichi M (1992) Morphoregulatory activities of E-cadherin and beta-1 integrins in colorectal tumour cells. Br J Cancer 66: 629-634
48. Qian F, Zhang ZC, Wu XF, Li YP, Xu Q (2005) Interaction between integrin alpha(5) and fibronectin is required for metastasis of B16F10 melanoma cells. Biochem Biophys Res Commun 333: 1269-1275
49. Romiti E, Vasta V, Meacci E, Farnararo M, Linke T, Ferlinz K, Sandhoff K, Bruni P (2000) Characterization of sphingomyelinase activity released by thrombin-stimulated platelets. Mol Cell Biochem 205: 75-81
50. Rotolo JA, Zhang J, Donepudi M, Lee H, Fuks Z, Kolesnick R (2005) Caspase-dependent and -independent activation of acid sphingomyelinase signaling. J Biol Chem 280: 26425-26434
51. Ruoslahti E, Giancotti FG (1989) Integrins and tumor cell dissemination. Cancer Cells 1: 119-126
52. 2+-stimulated sphingomyelinase is secreted by many cell types and is a product of the acid sphingomyelinase gene. J Biol Chem 271: 18431-18436
53. Schissel SL, Jiang X, Tweedie-Hardman J, Jeong T, Camejo EH, Najib J, Rapp JH, Williams KJ, Tabas I (1998a) Secretory sphingomyelinase, a product of the acid sphingomyelinase gene, can hydrolyze atherogenic lipoproteins at neutral pH. Implications for atherosclerotic lesion development. J Biol Chem 273: 2738-2746
54. Schissel SL, Keesler GA, Schuchman EH, Williams KJ, Tabas I (1998b) The cellular trafficking and zinc dependence of secretory and lysosomal sphingomyelinase, two products of the acid sphingomyelinase gene. J Biol Chem 273: 18250-18259
55. Schuchman EH, Suchi M, Takahashi T, Sandhoff K, Desnick RJ (1991) Human acid sphingomyelinase. Isolation, nucleotide sequence and expression of the full-length and alternatively spliced cDNAs. J Biol Chem 266: 8531-8539
56. Simon CG Jr, Chatterjee S, Gear AR (1998) Sphingomyelinase activity in human platelets. Thromb Res 90: 155-161
57. 2+-stimulated sphingomyelinase in fetal bovine serum. J Biol Chem 264: 5358-5363
58. Tohgo A, Tanaka N, Ashida S, Ogawa H (1984) Platelet-aggregating activities of metastasizing tumor cells. II. Variety of the aggregation mechanisms. Invasion Metastasis 4: 134-145
59. Wary KK, Mainiero F, Isakoff SJ, Marcantonio EE, Giancotti FG (1996) The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 87: 733-743
60. Wei Y, Yang X, Liu Q, Wilkins JA, Chapman HA (1999) A role for caveolin and the urokinase receptor in integrin-mediated adhesion and signaling. J Cell Biol 144: 1285-1294
61. Wiltrout RH, Herberman RB, Zhang SR, Chirigos MA, Ortaldo JR, Green K Jr, Talmadge JE (1985) Role of organ-associated NK cells in decreased formation of experimental metastases in lung and liver. J Immunol 134: 4267-4275
62. Xu M, Xia M, Li X-X, Han W-Q, Boini KM, Zhang F, Zhang Y, Ritter JK, Li P-L (2012) Requirement of translocated lysosomal V1 H(+)-ATPase for activation of membrane acid sphingomyelinase and raft clustering in coronary endothelial cells. Mol Biol Cell 23: 1546-1557
63. Yoshihara T, Esumi N, Humphries MJ, Imashuku S (1992) Unique expression of integrin fibronectin receptors in human neuroblastoma cell lines. Int J Cancer 51: 620-626