Assessment of the molecular expression and structure of gangliosides in brain metastasis of lung adenocarcinoma by an advanced approach based on fully automated chip-nanoelectrospray mass spectrometry

Journal of the American Society for Mass Spectrometry

Volumn 22, Issue 12, 2011, Pages 2145-2159

  Zamfir, Alina D ^a,b   Serb, Alina ^c   Vukeli, Željka ^d   Flangea, Corina ^a,b   Schiopu, Catalin ^b   Fabris, Dragana ^d   Kalanj Bognar, Svjetlana ^d   Capitan, Florina ^c   Sisu, Eugen ^c,e  

^a AUREL VLAICU UNIVERSITY OF ARAD   (Romania)

^b WEST UNIVERSITY OF TIMISOARA   (Romania)

^c VICTOR BABES UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^d UNIVERSITY OF ZAGREB   (Croatia)

^e ACADEMY OF ROMANIAN SCIENTISTS   (Romania)

Author keywords

Brain metastasis; Chip nanoelectrospray; Gangliosides; Lung adenocarcinoma; Quadrupole time of flight tandem mass spectrometry

Indexed keywords

ACETYLATION; BRAIN; CERAMIDES; CHAINS; DISSOCIATION; MASS SPECTROMETRY; MIXTURES; PATHOLOGY; TISSUE CULTURE; TUMORS;

BRAIN METASTASIS; GANGLIOSIDES; LUNG ADENOCARCINOMA; NANOELECTROSPRAY; QUADRUPOLE TIME-OF-FLIGHT TANDEM MASS SPECTROMETRIES;

TISSUE ENGINEERING;

CERAMIDE; GANGLIOSIDE; GANGLIOSIDE GD3; GANGLIOSIDE GM1; GANGLIOSIDE GM3; GANGLIOSIDE GM4; GLYCOSPHINGOLIPID; N ACETYLNEURAMINIC ACID; UNCLASSIFIED DRUG;

ACETYLATION; AGED; ANALYTIC METHOD; ARTICLE; BIOCHEMICAL COMPOSITION; BRAIN METASTASIS; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; FUCOSYLATION; HIGH PERFORMANCE THIN LAYER CHROMATOGRAPHY; HUMAN; HUMAN TISSUE; LUNG ADENOCARCINOMA; MALE; NANOCHIP; PROCESS OPTIMIZATION; QUANTITATIVE ANALYSIS; ROBOTICS; TANDEM MASS SPECTROMETRY;

EID: 84856147510     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-011-0250-5     Document Type: Article

References (64)

1. Sorensen, J. B., Hansen, H. H., Hansen, M., Dombernowsky, P.: Brain metastases in adenocarcinoma of the lung: frequency, risk groups, and prognosis. J. Clin. Oncol. 6, 1474-1480(1988) (Pubitemid 19089037)
2. Gow, C. H., Chien, C. R., Chang, Y. L., Chiu, Y. H., Kuo, S. H., Shih, J. Y., Chang, Y. C., Yu, C. J., Yang, C. H., Yang, P. C.: Radiotherapy in lung adenocarcinoma with brain metastases: effects of activating epidermal growth factor receptor mutations on clinical response. Clin. Cancer Res. 14, 162-168(2008)
3. Mehta, M. P., Rodrigus, P., Terhaard, C. H. J., Rao, A., Suh, J., Roa, W., Souhami, L., Bezjak, A., Leibenhaut, M., Komaki, R., Schultz, C., Timmerman, R., Curran, W., Smith, J., Phan, S. C., Miller, R. A., Renschler, M. F.: Survival and neurological outcomes in a randomized trial of motexafin gadolinium and whole-brain radiation therapy in brain metastases. J. Clin. Oncol. 21, 2529-2536(2003) (Pubitemid 46606335)
4. Ching, A. S. C., Chan, P. N., Ng, H. K., Tse, K. M., Chan, Y. L.: Isolated hemorrhagic brain metastasis from lung adenocarcinoma in a 68-yearold man. J. K. Coll. Radiol. 7, 140-144(2004) (Pubitemid 40766759)
5. Gavrilovic, I., Posner, J.: Brain metastases: epidemiology and pathophysiology. J. Neurooncol. 75, 5-14(2005) (Pubitemid 41548673)
6. Weil, R. J., Palmieri, D. C., Bronder, J. L., Stark, A. M., Steeg, P. S.: Breast cancer metastasis to the central nervous system. Am. J. Pathol. 167, 913-920(2005) (Pubitemid 41416243)
7. Ammirati, M., Cobbs, C. S., Linskey, M. E., Paleologos, N. A., Ryken, T. C., Burri, S. H., Asher, A. L., Loeffler, J. S., Robinson, P. D., Andrews, D. W., Gaspar, L. E., Kondziolka, D., McDermott, M., Mehta, M. P., Mikkelsen, T., Olson, J. J., Patchell, R. A., Kalkanis, S. N.: The role of retreatment in the management of recurrent/progressive brain metastases: a systematic review and evidence-based clinical practice guideline. J. Neurooncol. 96, 85-96(2010)
8. Gaspar, L. E., Mehta, M. P., Patchell, R. A., Burri, S. H., Robinson, P. D., Morris, R. E., Ammirati, M., Andrews, D. W., Asher, A. L., Cobbs, C. S., Kondziolka, D., Linskey, M. E., Loeffler, J. S., McDermott, M., Mikkelsen, T., Olson, J. J., Paleologos, N. A., Ryken, T. C., Kalkanis, S. N.: The role of whole brain radiation therapy in the management of newly diagnosed brain metastases: a systematic review and evidencebased clinical practice guideline. J. Neurooncol. 96, 17-32(2010)
9. Kalkanis, S. N., Kondziolka, D., Gaspar, L. E., Burri, S. H., Asher, A. L., Cobbs, C. S., Ammirati, M., Robinson, P. D., Andrews, D. W., Loeffler, J. S., McDermott, M., Mehta, M. P., Mikkelsen, T., Olson, J. J., Paleologos, N. A., Patchell, R. A., Ryken, T. C., Linskey, M. E.: The role of surgical resection in the management of newly diagnosed brain metastases: a systematic review and evidence-based clinical practice guideline. J. Neurooncol. 96, 33-43(2010)
10. Hakomori, S.: Glycosylation defining cancer malignancy: new wine in an old bottle. Proc. Natl. Acad. Sci. U. S. A. 99, 10231-10233(2002)
11. Kozbor, D.: Cancer vaccine with mimotopes of tumor-associated carbohydrated antygenes. Immunol. Res. 46, 23-31(2010)
12. Gorelik, E., Galili, U., Raz, A.: On the role of cell surface carbohydrates and their binding proteins (lectins) in tumor metastasis. Cancer Metastasis Rev. 20, 245-277(2001) (Pubitemid 34595270)
13. Colsch, B., Woods, A. S.: Localization and imaging of sialylated glycosphingolipids in brain tissue sections by MALDI mass spectrometry. Glycobiology 20, 661-667(2010)
14. Sonnino, S., Mauri, L., Chigorno, V., Prinetti, A.: Gangliosides as components of lipid membrane domains. Glycobiology 17, 1R-13R (2007) (Pubitemid 44932810)
15. Rösner, H.: Developmental expression and possible roles of gangliosides in brain development. Prog. Mol. Subcell. Biol. 32, 49-73(2003)
16. Lopez, P. H., Schnaar, R. L.: Gangliosides in cell recognition and membrane protein regulation. Curr. Opin. Struct. Biol. 19, 549-557(2009)
17. El-Abbadi, M., Seyfried, T. N., Yates, A. J., Orosz, C., Lee, M. C.: Ganglioside composition and histology of a spontaneous metastatic brain tumor in the VM mouse. Br. J. Cancer 85, 285-292(2001) (Pubitemid 32695753)
18. Müthing, J., Meisen, I., Kniep, B., Haier, J., Senninger, N, Neumann, U., Langer, M., Witthohn, K., Milosević, J., Peter-Katalinić, J.: Tumorassociated CD75s gangliosides and CD75s-bearing glycoproteins with Neu5Acα2-6Galβ1-4GlcNAc residues are receptors for the anticancer drug rViscumin. FASEB J. 19, 103-105(2005) (Pubitemid 40069932)
19. Distler, U., Souady, J., Hulsewig, M., Drmic-Hofman, I., Haier, J., Denz, A., Grutzmann, R., Pilarsky, C, Senninger, N, Dreisewerd, K., Berkenkamp, S., Schmidt, M. A., Peter-Katalinic, J., Muthing, J.: Tumor-associated CD75s-and iso-CD75s-gangliosides are potential targets for adjuvant therapy in pancreatic cancer. Mol. Cancer Ther. 7, 2464-2475(2008)
20. Kohla, G, Stockfleth, E., Schauer, R.: Gangliosides with O-acetylated sialic acids in tumors of neuroectodermal origin. Neurochem. Res. 27, 583-592(2002)
21. Papini, N., Anastasia, L., Tringali, C., Croci, G., Bresciani, R., Yamaguchi, K., Miyagi, T., Preti, A., Prinetti, A., Prioni, S., Sonnino, S., Tettamanti, G., Venerando, B., Monti, E.: The plasma membraneassociated sialidase MmNEU3 modifies the ganglioside pattern of adjacent cells supporting its involvement in cell-to-cell interactions. J. Biol. Chem. 279, 16989-16995(2004) (Pubitemid 38560452)
22. Tringali, C., Lupo, B., Anastasia, L., Papini, N., Monti, E., Bresciani, R., Tettamanti, G., Venerando, B.: Expression of sialidase Neu2 in leukemic K562 cells induces apoptosis by impairing Bcr-Abl/Src kinases signaling. J. Biol. Chem. 282, 14364-14372(2007) (Pubitemid 47100478)
23. Chen, H. H., Fukumoto, S., Furukawa, K., Nakao, A., Akiyama, S., Urano, T., Furukawa, K.: Suppression of lung metastasis of mouse Lewis lung cancer p29 with transfection of the ganglioside Gm2/Gd2 synthase gene. Int. J. Cancer 103, 169-176(2003) (Pubitemid 35461508)
24. Noguchi, M., Suzuki, T., Kabayama, K., Takahashi, H., Chiba, H., Shiratori, M., Abe, S., Watanabe, A., Satoh, M., Hasegawa, T., Tagami, S., Ishii, A., Saitoh, M., Kaneko, M., Iseki, K., Igarashi, Y., Inokuchi, J. I.: GM3 synthase gene is a novel biomarker for histologic classification and drug sensitivity against epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancer. Cancer Sci. 98, 1625-1632(2007) (Pubitemid 47308461)
25. Uemura, S., Kabayama, K., Noguchi, M., Igarashi, Y., Inokuchi, J. I.: Sialylation and sulfation of lactosylceramide distinctly regulate anchorage-independent growth, apoptosis, and gene expression in3LL Lewis lung carcinoma cells. Glycobiology 13, 207-216(2003) (Pubitemid 36511756)
26. Zhang, Q., Furukawa, K., Chen, H. H., Sakakibara, T., Urano, T., Furukawa, K: Metastatic potential of mouse Lewis lung cancer cells is regulated via ganglioside GM1 by modulating the matrix metalloprotease-9 localization in lipid rafts. J. Biol. Chem. 281, 18145-18155(2006) (Pubitemid 44035614)
27. Tokuda, N., Zhang, Q., Yoshida, S., Kusunoki, S., Urano, T., Furukawa, K., Furukawa, K.: Genetic mechanisms for the synthesis of fucosyl GM1 in small cell lung cancer cell lines. Glycobiology 16, 916-925(2006) (Pubitemid 44390934)
28. Nagorny, P., Kim, W. H., Wan, Q., Lee, D., Danishefsky, S. J.: On the emerging role of chemistry in the fashioning of biologics: synthesis of a bidomainal fucosyl GM1-based vaccine for the treatment of small cell lung cancer. J. Org. Chem. 74, 5157-5162(2009)
29. Diaz, Y., Gonzalez, A., Lopez, A., Perez, R., Vazquez, A. M., Montero, E.: Anti-ganglioside anti-idiotypic monoclonal antibody-based cancer vaccine induces apoptosis and antiangiogenic effect in a metastatic lung carcinoma. Cancer Immunol. Immunother. 58, 1117-1128(2009)
30. Fredman, P., Brezicka, T., Holmgren, J., Lindholm, L., Nilsson, O., Svennerholm, L.: Binding specificity of monoclonal antibodies to ganglioside Fuc-GM. Biochim. Biophys. Acta 75, 316-323(1986) (Pubitemid 16149054)
31. Muthing, J., Distler, U: Advances on the compositional analysis of glycosphingolipids combining thin-layer chromatography with mass spectrometry. Mass Spectrom. Rev. 29, 425-479(2010)
32. Ting, Y. S., Shaffer, S. A., Jones, J. W., Ng, W. V., Ernst, R. K., Goodlett, D. R.: Automated lipid A structure assignemnt from hierachical tandem mass spectrometry data. J. Am. Soc. Mass Spectrom. 22, 856-866(2011)
33. Jones, J. W., Cohen, I. E., Turecek, F., Goodlett, D. R., Ernst, R. K.: Comprehensive structure characterization of lipid A extracted from Yersinia pestis for determination of its phosphorilation configuration. J. Am. Soc. Mass Spectrom. 21, 785-799(2010)
34. Zamfir, A. D., Flangea, C., Altmann, F., Rizzi, A.: Glycosylation analysis of proteins, proteoglycans, and glycolipids using capillary electrophoresis and mass spectrometry. Adv. Chromatogr. 49, 135-194(2011)
35. Vukelić, Z., Kalanj-Bognar, S., Froesch, M., Bîndila, L., Radić, B., Allen, M., Peter-Katalinić, J., Zamfir, A. D.: Human gliosarcomaassociated ganglioside composition is complex and distinctive as evidenced by high-performance mass spectrometric determination and structural characterization. Glycobiology 17, 504-515(2007) (Pubitemid 47049938)
36. Zamfir, A., Vukelić, Z., Bindila, L., Peter-Katalinic, J., Almeida, R., Sterling, A., Allen, M.: Fully-automated chip-based nanoelectrospray tandem mass spectrometry of gangliosides from human cerebellum. J. Am. Soc. Mass. Spectrom. 15, 1649-1657(2004) (Pubitemid 39433859)
37. Vukelić, Z., Zarei, M., Peter-Katalinić, J., Zamfir, A. D.: Analysis of human hippocampus gangliosides by fully-automated chip-based nanoelectrospray tandem mass spectrometry. J. Chromatogr. A 1130, 238-245(2006) (Pubitemid 44441308)
38. Serb, A., Schiopu, C., Flangea, C., Vukelić, Ž., Sisu, E., Zagrean, L., Zamfir, A. D.: High-throughput analysis of gangliosides in defined regions of fetal brain by fully automated chip-based nanoelectrospray ionization multistage mass spectrometry. Eur. J. Mass Spectrom. 15, 541-553(2009)
39. Serb, A., Schiopu, C., Flangea, C., Sisu, E., Zamfir, A. D.: Top-down glycolipidomics: fragmentation analysis of ganglioside oligosaccharide core and ceramide moiety by chip-nanoelectrospray collision-induced dissociation MS (2)-MS (6). J. Mass Spectrom. 44, 1434-1442(2009)
40. Schiopu, C., Flangea, C., Capitan, F., Serb, A., Vukelić, Ž., Kalanj-Bognar, S., Sisu, E., Przybylski, M., Zamfir, A. D.: Determination of ganglioside composition and structure in human brain hemangioma by chip-based nanoelectrospray ionisation tandem mass spectrometry. Anal. Bioanal Chem. 395, 2465-2477(2009)
41. Almeida, R., Mosoarca, C., Chirita, M., Udrescu, V., Dinca, N., Vukelić, Z., Allen, M., Zamfir, A. D.: Coupling of fully automated chipbased electrospray ionization to high-capacity ion trap mass spectrometer for ganglioside analysis. Anal. Biochem. 378, 43-52(2008)
42. Dall'Olio, F.: The sialyl-alpha2, 6-lactosaminyl-structure: biosynthesis and functional role. Glycoconj J 17, 669-676(2000) (Pubitemid 32493944)
43. Svennerholm, L., Fredman, P.: A procedure for the quantitative isolation of brain gangliosides. Biochim. Biophys. Acta 617, 97-109(1980) (Pubitemid 10185886)
44. Vukelić, Ž., Metelmann, W., Müthing, J., Kos, M., Peter-Katalinić, J.: Anencephaly: structural characterization of gangliosides in defined brain regions. Biol. Chem. 382, 259-274(2001) (Pubitemid 32243934)
45. Svennerholm, L.: Quantitative estimation of sialic acids II. A colorimetric resorcinol-hydrochloric acid method. Biochim. Biophys. Acta 24, 104-111(1957)
46. Miettinen, T., Takki-Luukkainen, I. T.: Use of buthylacetate in determination of sialic acid. Acta Chem. Scand. 13, 656-658(1959)
47. Trbojević-Cepe, M., Kracun, I.: Determination of gangliosides in human cerebrospinal fluid by high-performance thin-layer chromatography and direct densitometry. J. Clin. Chem. Clin. Biochem. 8, 863-872(1990) (Pubitemid 20374386)
48. Domon, B., Costello, C. E.: A systematic nomenclature for carbohydrate fragmentation in FAB-MS/MS spectra of glycoconjugates. Glycoconj. J. 5, 397-409(1988) (Pubitemid 19031141)
49. Ann, Q., Adams, J.: Structure determination of ceramides and neutral glycosphingolipids by collisional activation of [M+Li]+ ions. J. Am. Soc. Mass Spectrom. 3, 260-266(1992)
50. Nilsson, O., Svennerholm, L.: Characterization and quantitative determination of gangliosides and neutral glycosphingolipids in human liver. J. Lipid Res. 23, 327-334(1982) (Pubitemid 12106211)
51. Keranen, A.: Gangliosides of the human gastrointestinal mucosa. Biochim. Biophys. Acta 409, 320-328(1975)
52. Narasimhan, R., Murray, R. K.: Neutral glycosphingolipids and gangliosides of human lung and lung tumours. Biochem J. 179, 199-211(1979) (Pubitemid 9177048)
53. Metelmann, W., Vukelić, Ž., Peter-Katalinić, J.: Nano-electrospray ionization time-of-flight mass spectrometry of gangliosides from human brain tissue. J. Mass Spectrom. 36, 21-29(2001)
54. Vukelić, Z., Zamfir, A. D., Bindila, L., Froesch, M., Peter-Katalinić, J., Usuki, S., Yu, R. K.: Screening and sequencing of complex sialylated and sulfated glycosphingolipid mixtures by negative ion electro-spray Fourier transform ion cyclotron resonance mass spectrometry. J. Am. Soc. Mass Spectrom. 16, 571-580(2005) (Pubitemid 40410042)
55. Iwamori, M., Domino, S. E.: Tissue-specific loss of fucosylated glycolipids in mice with targeted deletion of alpha (1, 2) fucosyltransferase genes. Biochem. J. 380, 75-81(2004) (Pubitemid 38725731)
56. Hamasaki, H., Aoyagi, M., Kasama, T., Handa, S., Hirakawa, K., Taki, T.: GT1b in human metastatic brain tumors: GT1b as a brain metastasisassociated ganglioside. Biochim. Biophys. Acta 1437, 93-99(1999) (Pubitemid 29242907)
57. Brady, R. O., Fishman, P. H.: Biosynthesis of glycolipids in virustransformed cells. Biochim. Biophys. Acta 355, 121-148(1974)
58. Hakomori, S.: Structures and organization of cell surface glycolipids dependency on cell growth and malignant transformation. Biochim. Biophys. Acta 417, 56-89(1975)
59. Mugnai, G., Coppini, R., Tombaccini, D., Fallani, A., Ruggieri, S.: Neutral glycolipids and gangliosides of concanavalin A-selected SV3T3 revertant cells and of normal and SV40-transformed Balb/c 3 T3 cells. Biochem. J. 193, 1025-1028(1981) (Pubitemid 11119438)
60. Calorini, L., Fallani, A., Tombaccini, D., Barletta, E., Mugnai, G., Di Renzo, M. F., Comoglio, P. M., Ruggieri, S.: Lipid characteristics of RSV-transformed Balb/c 3 T3 cell lines with different spontaneous metastatic potentials. Lipids 24, 685-690(1989) (Pubitemid 19221820)
61. Ruggieri, S., Mugnai, G., Mannini, A., Calorini, L., Fallani, A., Barletta, E., Mannori, G., Cecconi, O.: Lipid characteristics in metastatic cells. Clin. Exp. Metast. 17, 271-276(1999) (Pubitemid 29477571)
62. Mukherjee, P., Faber, A. C., Shelton, L. M., Baek, R. C., Chiles, T. C., Seyfried, T. N.: Thematic review series: sphingolipids. Ganglioside GM3 suppresses the proangiogenic effects of vascular endothelial growth factor and ganglioside GD1a. J. Lipid Res. 49, 929-938(2008)
63. Petro, K. A., Schengrund, C. L.: Membrane raft disruption promotes axonogenesis in N2a neuroblastoma cells. Neurochem. Res. 34, 29-37(2009)
64. Koochekpour, S., Merzak, A., Pilkington, G. J.: Vascular endothelial growth factor production is stimulated by gangliosides and TGF-β isoforms in human glioma cells in vitro. Cancer Lett. 102, 209-215(1996) (Pubitemid 26097822)