Cell density-dependent membrane distribution of ganglioside GM3 in melanoma cells
Tóm tắt
Monosialoganglioside GM3 is the simplest ganglioside involved in various cellular signaling. Cell surface distribution of GM3 is thought to be crucial for the function of GM3, but little is known about the cell surface GM3 distribution. It was shown that anti-GM3 monoclonal antibody binds to GM3 in sparse but not in confluent melanoma cells. Our model membrane study evidenced that monoclonal anti-GM3 antibodies showed stronger binding when GM3 was in less fluid membrane environment. Studies using fluorescent GM3 analogs suggested that GM3 was clustered in less fluid membrane. Moreover, fluorescent lifetime measurement showed that cell surface of high density melanoma cells is more fluid than that of low density cells. Lipidomics and fatty acid supplementation experiment suggested that monounsaturated fatty acid-containing phosphatidylcholine contributed to the cell density-dependent membrane fluidity. Our results indicate that anti-GM3 antibody senses GM3 clustering and the number and/or size of GM3 cluster differ between sparse and confluent melanoma cells.
Tài liệu tham khảo
Zheng M, Fang H, Tsuruoka T, Tsuji T, Sasaki T, Hakomori S (1993) Regulatory role of GM3 ganglioside in alpha 5 beta 1 integrin receptor for fibronectin-mediated adhesion of FUA169 cells. J Biol Chem 268(3):2217–2222. https://doi.org/10.1016/S0021-9258(18)53984-3
Kabayama K, Sato T, Saito K, Loberto N, Prinetti A, Sonnino S, Kinjo M, Igarashi Y, Inokuchi J (2007) Dissociation of the insulin receptor and caveolin-1 complex by ganglioside GM3 in the state of insulin resistance. Proc Natl Acad Sci USA 104(34):13678–13683. https://doi.org/10.1073/pnas.0703650104
Coskun U, Grzybek M, Drechsel D, Simons K (2011) Regulation of human EGF receptor by lipids. Proc Natl Acad Sci USA 108(22):9044–9048. https://doi.org/10.1073/pnas.1105666108
Nakano M, Hanashima S, Hara T, Kabayama K, Asahina Y, Hojo H, Komura N, Ando H, Nyholm TKM, Slotte JP, Murata M (2021) FRET detects lateral interaction between transmembrane domain of EGF receptor and ganglioside GM3 in lipid bilayers. Biochim Biophys Acta 1863:183623. https://doi.org/10.1016/j.bbamem.2021.183623
Inokuchi JI, Kanoh H, Inamori KI, Nagafuku M, Nitta T, Fukase K (2021) Homeostatic and pathogenic roles of the GM3 ganglioside. FEBS J 289:5152–5165. https://doi.org/10.1111/febs.16076
Hirabayashi Y, Hamaoka A, Matsumoto M, Matsubara T, Tagawa M, Wakabayashi S, Taniguchi M (1985) Syngeneic monoclonal antibody against melanoma antigen with interspecies cross-reactivity recognizes GM3, a prominent ganglioside of B16 melanoma. J Biol Chem 260(24):13328–13333. https://doi.org/10.1016/S0021-9258(17)38873-7
Kotani M, Ozawa H, Kawashima I, Ando S, Tai T (1992) Generation of one set of monoclonal antibodies specific for a-pathway ganglio-series gangliosides. Biochim Biophys Acta 1117(1):97–103. https://doi.org/10.1016/0304-4165(92)90168-t
Dohi T, Nores G, Hakomori S (1988) An IgG3 monoclonal antibody established after immunization with GM3 lactone: immunochemical specificity and inhibition of melanoma cell growth in vitro and in vivo. Cancer Res 48:5680–5685
Gomez-Mouton C, Abad JL, Mira E, Lacalle RA, Gallardo E, Jimenez-Baranda S, Illa I, Bernad A, Manes S, Martinez AC (2001) Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad Sci USA 98:9642–9647. https://doi.org/10.1073/pnas.171160298
Janich P, Corbeil D (2007) GM1 and GM3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells. FEBS Lett 581:1783–1787. https://doi.org/10.1016/j.febslet.2007.03.065
Fujita A, Cheng J, Hirakawa M, Furukawa K, Kusunoki S, Fujimoto T (2007) Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Mol Biol Cell 18:2112–2122. https://doi.org/10.1091/mbc.e07-01-00712
Chigorno V, Palestini P, Sciannamblo M, Dolo V, Pavan A, Tettamanti G, Sonnino S (2000) Evidence that ganglioside enriched domains are distinct from caveolae in MDCK II and human fibroblast cells in culture. Eur J Biochem 267(13):4187–4197. https://doi.org/10.1046/j.1432-1327.2000.01454.x
Cutillo G, Saariaho AH, Meri S (2020) Physiology of gangliosides and the role of antiganglioside antibodies in human diseases. Cell Mol Immunol 17:313–322. https://doi.org/10.1038/s41423-020-0388-9
Willison HJ, Yuki N (2002) Peripheral neuropathies and anti-glycolipid antibodies. Brain 125:2591–2625. https://doi.org/10.1093/brain/awf272
Lloyd KO, Gordon CM, Thampoe IJ, DiBenedetto C (1992) Cell surface accessibility of individual gangliosides in malignant melanoma cells to antibodies is influenced by the total ganglioside composition of the cells. Cancer Res 52:4948–4953
Greenshields KN, Halstead SK, Zitman FM, Rinaldi S, Brennan KM, O’Leary C, Chamberlain LH, Easton A, Roxburgh J, Pediani J, Furukawa K, Furukawa K, Goodyear CS, Plomp JJ, Willison HJ (2009) The neuropathic potential of anti-GM1 autoantibodies is regulated by the local glycolipid environment in mice. J Clin Invest 119:595–610. https://doi.org/10.1172/JCI37338
Lingwood D, Binnington B, Rog T, Vattulainen I, Grzybek M, Coskun U, Lingwood CA, Simons K (2011) Cholesterol modulates glycolipid conformation and receptor activity. Nat Chem Biol 7:260–262. https://doi.org/10.1038/nchembio.551
Sakiyama H, Takahashi T, Hirabayashi Y, Taniguchi M (1987) Change in the topographical distribution of GM3 during cell spreading and growth: immunostaining with monoclonal antibody against GM3. Cell Struct Funct 12:93–105. https://doi.org/10.1247/csf.12.93
Tatewaki K, Yamaki T, Maeda Y, Tobioka H, Piao H, Yu H, Ibayashi Y, Sawada N, Hashi K (1997) Cell density regulates crypticity of GM3 ganglioside on human glioma cells. Exp Cell Res 233:145–154. https://doi.org/10.1006/excr.1997.3563
Kotani M, Kawashima I, Ozawa H, Ogura K, Ishizuka I, Terashima T, Tai T (1994) Immunohistochemical localization of minor gangliosides in the rat central nervous system. Glycobiology 4:855–865. https://doi.org/10.1093/glycob/4.6.855
Sorice M, Parolini I, Sansolini T, Garofalo T, Dolo V, Sargiacomo M, Tai T, Peschle C, Torrisi MR, Pavan A (1997) Evidence for the existence of ganglioside-enriched plasma membrane domains in human peripheral lymphocytes. J Lipid Res 38:969–980. https://doi.org/10.1016/S0022-2275(20)37221-7
Misasi R, Sorice M, Garofalo T, Griggi T, Campana WM, Giammatteo M, Pavan A, Hiraiwa M, Pontieri GM, O’Brien JS (1998) Colocalization and complex formation between prosaposin and monosialoganglioside GM3 in neural cells. J Neurochem 71:2313–2321. https://doi.org/10.1046/j.1471-4159.1998.71062313.x
Garofalo T, Lenti L, Longo A, Misasi R, Mattei V, Pontieri GM, Pavan A, Sorice M (2002) Association of GM3 with Zap-70 induced by T cell activation in plasma membrane microdomains: GM3 as a marker of microdomains in human lymphocytes. J Biol Chem 277:11233–11238. https://doi.org/10.1074/jbc.M109601200
Chen Y, Qin J, Chen ZW (2008) Fluorescence-topographic NSOM directly visualizes peak-valley polarities of GM1/GM3 rafts in cell membrane fluctuations. J Lipid Res 49:2268–2275. https://doi.org/10.1194/jlr.D800031-JLR200
Murate M, Abe M, Kasahara K, Iwabuchi K, Umeda M, Kobayashi T (2015) Transbilayer distribution of lipids at nano scale. J Cell Sci 128:1627–1638. https://doi.org/10.1242/jcs.163105
Marsh D (2013) Handbook of lipid bilayers, 2nd edn. CRC Press, Boca Raton
Taniguchi M, Wakabayashi S (1984) Shared antigenic determinant expressed on various mammalian melanoma cells. Gan 75:418–426
Komura N, Suzuki KG, Ando H, Konishi M, Koikeda M, Imamura A, Chadda R, Fujiwara TK, Tsuboi H, Sheng R, Cho W, Furukawa K, Furukawa K, Yamauchi Y, Ishida H, Kusumi A, Kiso M (2016) Raft-based interactions of gangliosides with a GPI-anchored receptor. Nat Chem Biol 12:402–410. https://doi.org/10.1038/nchembio.2059
MacDonald RI (1990) Characteristics of self-quenching of the fluorescence of lipid-conjugated rhodamine in membranes. J Biol Chem 265:13533–13539. https://doi.org/10.1016/S0021-9258(18)77380-77388
Elvington SM, Nichols JW (2007) Spontaneous, intervesicular transfer rates of fluorescent, acyl chain-labeled phosphatidylcholine analogs. Biochim Biophys Acta 1768:502–508. https://doi.org/10.1016/j.bbamem.2006.11.013
Coste V, Puff N, Lockau D, Quinn PJ, Angelova MI (2006) Raft-like domain formation in large unilamellar vesicles probed by the fluorescent phospholipid analogue, C12NBD-PC. Biochim Biophys Acta 1758:460–467. https://doi.org/10.1016/j.bbamem.2006.03.003
Puff N, Watanabe C, Seigneuret M, Angelova MI, Staneva G (2014) Lo/Ld phase coexistence modulation induced by GM1. Biochim Biophys Acta 1838:2105–2114. https://doi.org/10.1016/j.bbamem.2014.05.002
Xu X, London E (2000) The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry 39(5):843–849. https://doi.org/10.1021/bi992543v
Tanaka KA, Suzuki KG, Shirai YM, Shibutani ST, Miyahara MS, Tsuboi H, Yahara M, Yoshimura A, Mayor S, Fujiwara TK, Kusumi A (2010) Membrane molecules mobile even after chemical fixation. Nat Methods 7:865–866. https://doi.org/10.1038/nmeth.f.314
Brady RO, Kanfer JN, Mock MB, Fredrickson DS (1966) The metabolism of sphingomyelin. II. Evidence of an enzymatic deficiency in Niemann-Pick diseaese. Proc Natl Acad Sci USA 55:366–369. https://doi.org/10.1073/pnas.55.2.366
Shynkar VV, Klymchenko AS, Kunzelmann C, Duportail G, Muller CD, Demchenko AP, Freyssinet JM, Mely Y (2007) Fluorescent biomembrane probe for ratiometric detection of apoptosis. J Am Chem Soc 129(7):2187–2193. https://doi.org/10.1021/ja068008h
Kilin V, Glushonkov O, Herdly L, Klymchenko A, Richert L, Mely Y (2015) Fluorescence lifetime imaging of membrane lipid order with a ratiometric fluorescent probe. Biophys J 108:2521–2531. https://doi.org/10.1016/j.bpj.2015.04.003
Shimada Y, Maruya M, Iwashita S, Ohno-Iwashita Y (2002) The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains. Eur J Biochem 269:6195–6203. https://doi.org/10.1046/j.1432-1033.2002.03338.x
Kishimoto T, Tomishige N, Murate M, Ishitsuka R, Schaller H, Mely Y, Ueda K, Kobayashi T (2020) Cholesterol asymmetry at the tip of filopodia during cell adhesion. FASEB J 34:6185–6197. https://doi.org/10.1096/fj.201900065RR
Verkleij AJ, Zwaal RF, Roelofsen B, Comfurius P, Kastelijn D, van Deenen LL (1973) The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy. Biochim Biophys Acta 323:178–193. https://doi.org/10.1016/0005-2736(73)90143-0
Doktorova M, Symons JL, Levental I (2020) Structural and functional consequences of reversible lipid asymmetry in living membranes. Nat Chem Biol 16:1321–1330. https://doi.org/10.1038/s41589-020-00688-0
Blom TS, Koivusalo M, Kuismanen E, Kostiainen R, Somerharju P, Ikonen E (2001) Mass spectrometric analysis reveals an increase in plasma membrane polyunsaturated phospholipid species upon cellular cholesterol loading. Biochemistry 40:14635–14644. https://doi.org/10.1021/bi0156714
Samuel D, Paris S, Ailhaud G (1976) Uptake and metabolism of fatty acids and analogues by cultured cardiac cells from chick embryo. Eur J Biochem 64:583–595. https://doi.org/10.1111/j.1432-1033.1976.tb10338.x
Rohwedder A, Zhang Q, Rudge SA, Wakelam MJ (2014) Lipid droplet formation in response to oleic acid in Huh-7 cells is mediated by the fatty acid receptor FFAR4. J Cell Sci 127:3104–3115. https://doi.org/10.1242/jcs.145854
Targett-Adams P, Chambers D, Gledhill S, Hope RG, Coy JF, Girod A, McLauchlan J (2003) Live cell analysis and targeting of the lipid droplet-binding adipocyte differentiation-related protein. J Biol Chem 278:15998–16007. https://doi.org/10.1074/jbc.M211289200
Wang H, Wei E, Quiroga AD, Sun X, Touret N, Lehner R (2010) Altered lipid droplet dynamics in hepatocytes lacking triacylglycerol hydrolase expression. Mol Biol Cell 21:1991–2000. https://doi.org/10.1091/mbc.e09-05-0364
Homan R, Grossman JE, Pownall HJ (1991) Differential effects of eicosapentaenoic acid and oleic acid on lipid synthesis and secretion by HepG2 cells. J Lipid Res 32:231–241. https://doi.org/10.1016/S0022-2275(20)42084-X
Schroedl NA, Hartzell CR (1984) Preferential distribution of non-esterified fatty acids to phosphatidylcholine in the neonatal mammalian myocardium. Biochem J 224:651–659. https://doi.org/10.1042/bj2240651
Wang S, McLeod RS, Gordon DA, Yao Z (1996) The microsomal triglyceride transfer protein facilitates assembly and secretion of apolipoprotein B-containing lipoproteins and decreases cotranslational degradation of apolipoprotein B in transfected COS-7 cells. J Biol Chem 271:14124–14133. https://doi.org/10.1074/jbc.271.24.14124
Caviglia JM, De Gomez Dumm IN, Coleman RA, Igal RA (2004) Phosphatidylcholine deficiency upregulates enzymes of triacylglycerol metabolism in CHO cells. J Lipid Res 45:1500–1509. https://doi.org/10.1194/jlr.M400079-JLR200
Besson N, Hullin-Matsuda F, Makino A, Murate M, Lagarde M, Pageaux JF, Kobayashi T, Delton-Vandenbroucke I (2006) Selective incorporation of docosahexaenoic acid into lysobisphosphatidic acid in cultured THP-1 macrophages. Lipids 41:189–196. https://doi.org/10.1007/s11745-006-5087-5
Maggio B, Ariga T, Sturtevant JM, Yu RK (1985) Thermotropic behavior of binary mixtures of dipalmitoylphosphatidylcholine and glycosphingolipids in aqueous dispersions. Biochim Biophys Acta 818:1–12. https://doi.org/10.1016/0005-2736(85)90131-2
Matuoka S, Akiyama M, Yamada H, Tsuchihashi K, Gasa S (2003) Phase behavior in multilamellar vesicles of DPPC containing ganglioside GM3 with a C18:1 sphingoid base and a 24:0 acyl chain (GM3(18,24)) observed by X-ray diffraction. Chem Phys Lipids 123:19–29. https://doi.org/10.1016/s0009-3084(02)00128-7
Maggio B, Ariga T, Sturtevant JM, Yu RK (1985) Thermotropic behavior of glycosphingolipids in aqueous dispersions. Biochemistry 24:1084–1092. https://doi.org/10.1016/0005-2736(85)90131-2
Maulik PR, Shipley GG (1996) N-palmitoyl sphingomyelin bilayers: structure and interactions with cholesterol and dipalmitoylphosphatidylcholine. Biochemistry 35:8025–8034. https://doi.org/10.1021/bi9528356
Sarmento MJ, Owen MC, Ricardo JC, Chmelova B, Davidovic D, Mikhalyov I, Gretskaya N, Hof M, Amaro M, Vacha R, Sachl R (2021) The impact of the glycan headgroup on the nanoscopic segregation of gangliosides. Biophys J 120:5530–5543. https://doi.org/10.1016/j.bpj.2021.11.017
Palestini P, Pitto M, Sonnino S, Omodeo-Sale MF, Masserini M (1995) Spontaneous transfer of GM3 ganglioside between vesicles. Chem Phys Lipids 77:253–260. https://doi.org/10.1016/0009-3084(95)02474-w
Brotherus J, Renkonen O (1977) Phospholipids of subcellular organelles isolated from cultured BHK cells. Biochim Biophys Acta 486:243–253. https://doi.org/10.1016/0005-2760(77)90020-0
Valiente O, Mauri L, Casellato R, Fernandez LE, Sonnino S (2001) Preparation of deacetyl-, lyso-, and deacetyl-lyso-GM(3) by selective alkaline hydrolysis of GM3 ganglioside. J Lipid Res 42(8):1318–1324. https://doi.org/10.1016/S0022-2275(20)31583-2
Abe M, Makino A, Hullin-Matsuda F, Kamijo K, Ohno-Iwashita Y, Hanada K, Mizuno H, Miyawaki A, Kobayashi T (2012) A role for sphingomyelin-rich lipid domains in the accumulation of phosphatidylinositol 4,5-bisphosphate to the cleavage furrow during cytokinesis. Mol Cell Biol 32:1396–1407. https://doi.org/10.1128/MCB.06113-11
Yamaji-Hasegawa A, Makino A, Baba T, Senoh Y, Kimura-Suda H, Sato SB, Terada N, Ohno S, Kiyokawa E, Umeda M, Kobayashi T (2003) Oligomerization and pore formation of a sphingomyelin-specific toxin, lysenin. J Biol Chem 278(25):22762–22770. https://doi.org/10.1074/jbc.M213209200
Kremer JM, Esker MW, Pathmamanoharan C, Wiersema PH (1977) Vesicles of variable diameter prepared by a modified injection method. Biochemistry 16:3932–3935. https://doi.org/10.1021/bi00636a033
Kobayashi T, Pagano RE (1988) ATP-dependent fusion of liposomes with the Golgi apparatus of perforated cells. Cell 55:797–805. https://doi.org/10.1016/0092-8674(88)90135-3
Ishitsuka R, Yamaji-Hasegawa A, Makino A, Hirabayashi Y, Kobayashi T (2004) A lipid-specific toxin reveals heterogeneity of sphingomyelin-containing membranes. Biophys J 86:296–307. https://doi.org/10.1016/S0006-3495(04)74105-3
Kobayashi T, Beuchat MH, Lindsay M, Frias S, Palmiter RD, Sakuraba H, Parton RG, Gruenberg J (1999) Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat Cell Biol 1:113–118. https://doi.org/10.1038/10084
Makino A, Abe M, Murate M, Inaba T, Yilmaz N, Hullin-Matsuda F, Kishimoto T, Schieber NL, Taguchi T, Arai H, Anderluh G, Parton RG, Kobayashi T (2015) Visualization of the heterogeneous membrane distribution of sphingomyelin associated with cytokinesis, cell polarity, and sphingolipidosis. FASEB J 29:477–493. https://doi.org/10.1096/fj.13-247585
Clamme JP, Azoulay J, Mely Y (2003) Monitoring of the formation and dissociation of polyethylenimine/DNA complexes by two photon fluorescence correlation spectroscopy. Biophys J 84:1960–1968. https://doi.org/10.1016/S0006-3495(03)75004-8
Azoulay J, Clamme JP, Darlix JL, Roques BP, Mely Y (2003) Destabilization of the HIV-1 complementary sequence of TAR by the nucleocapsid protein through activation of conformational fluctuations. J Mol Biol 326:691–700. https://doi.org/10.1016/s0022-2836(02)01430-4
Warren SC, Margineanu A, Alibhai D, Kelly DJ, Talbot C, Alexandrov Y, Munro I, Katan M, Dunsby C, French PM (2013) Rapid global fitting of large fluorescence lifetime imaging microscopy datasets. PLoS ONE 8:e70687. https://doi.org/10.1371/journal.pone.0070687
Becker W, Shcheslavkiy V, Frere S, Slutsky I (2014) Spatially resolved recording of transient fluorescence-lifetime effects by line-scanning TCSPC. Microsc Res Tech 77(3):216–224. https://doi.org/10.1002/jemt.22331
Yamaji-Hasegawa A, Murate M, Inaba T, Dohmae N, Sato M, Fujimori F, Sako Y, Greimel P, Kobayashi T (2022) A novel sterol-binding protein reveals heterogeneous cholesterol distribution in neurite outgrowth and in late endosomes/lysosomes. Cellul Mol Life Sci 79:324. https://doi.org/10.1007/s00018-022-04339-6
Yokoyama K, Suzuki M, Kawashima I, Karasawa K, Nojima S, Enomoto T, Tai T, Suzuki A, Setaka M (1997) Changes in composition of newly synthesized sphingolipids of HeLa cells during the cell cycle – suppression of sphingomyelin and higher-glycosphingolipid synthesis and accumulation of ceramide and glucosylceramide in mitotic cells. Eur J Biochem 249:450–455. https://doi.org/10.1111/j.1432-1033.1997.00450.x
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917. https://doi.org/10.1139/o59-099