42
Views
51
CrossRef citations to date
0
Altmetric
Article

Regulation of Cell Migration by Sphingomyelin Synthases: Sphingomyelin in Lipid Rafts Decreases Responsiveness to Signaling by the CXCL12/CXCR4 Pathway

, , , , , , , , , , & show all
Pages 3242-3252 | Received 25 Jan 2012, Accepted 30 May 2012, Published online: 20 Mar 2023

REFERENCES

  • Albi E, Cataldi S, Rossi G, Magni MV. 2003. A possible role of cholesterol-sphingomyelin/phosphatidylcholine in nuclear matrix during rat liver regeneration. J. Hepatol. 38:623–628.
  • Anderson RG, Jacobson K. 2002. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296:1821–1825.
  • Angers S, et al. 2000. Detection of beta 2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc. Natl. Acad. Sci. U. S. A. 97:3684–3689.
  • Babcock GJ, Farzan M, Sodroski J. 2003. Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor. J. Biol. Chem. 278:3378–3385.
  • Balabanian K, et al. 2005. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J. Biol. Chem. 280:35760–35766.
  • Balkwill F. 2004. The significance of cancer cell expression of the chemokine receptor CXCR4. Semin. Cancer Biol. 14:171–179.
  • Bligh EG, Dyer WJ. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911–917.
  • Brown D. 2002. Structure and function of membrane rafts. Int. J. Med. Microbiol. 291:433–437.
  • Burger JA, Kipps TJ. 2006. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 107:1761–1767.
  • Burns JM, et al. 2006. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J. Exp. Med. 203:2201–2213.
  • Cadena DL, Gill GN. 1992. Receptor tyrosine kinases. FASEB J. 6:2332–2337.
  • Charruyer A, et al. 2008. Decreased ceramide transport protein (CERT) function alters sphingomyelin production following UVB irradiation. J. Biol. Chem. 283:16682–16692.
  • Ding T, et al. 2008. SMS overexpression and knockdown: impact on cellular sphingomyelin and diacylglycerol metabolism, and cell apoptosis. J. Lipid Res. 49:376–385.
  • Dinger MC, Bader JE, Kobor AD, Kretzschmar AK, Beck-Sickinger AG. 2003. Homodimerization of neuropeptide y receptors investigated by fluorescence resonance energy transfer in living cells. J. Biol. Chem. 278:10562–10571.
  • Dolgachev V, et al. 2004. De novo ceramide accumulation due to inhibition of its conversion to complex sphingolipids in apoptotic photosensitized cells. J. Biol. Chem. 279:23238–23249.
  • Griner EM, Kazanietz MG. 2007. Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer. 7:281–294.
  • Hannun YA, Obeid LM. 2008. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9:139–150.
  • Heakal Y, Kester M. 2009. Nanoliposomal short-chain ceramide inhibits agonist-dependent translocation of neurotensin receptor 1 to structured membrane microdomains in breast cancer cells. Mol. Cancer Res. 7:724–734.
  • Horuk R. 2001. Chemokine receptors. Cytokine Growth Factor Rev. 12:313–335.
  • Huitema K, van den Dikkenberg J, Brouwers JF, Holthuis JC. 2004. Identification of a family of animal sphingomyelin synthases. EMBO J. 23:33–44.
  • Isik N, Hereld D, Jin T. 2008. Fluorescence resonance energy transfer imaging reveals that chemokine-binding modulates heterodimers of CXCR4 and CCR5 receptors. PLoS One 3:e3424. https://doi.org/10.1371/journal.pone.0003424.
  • Issafras H, et al. 2002. Constitutive agonist-independent CCR5 oligomerization and antibody-mediated clustering occurring at physiological levels of receptors. J. Biol. Chem. 277:34666–34673.
  • Jin ZX, et al. 2008. Impaired TCR signaling through dysfunction of lipid rafts in sphingomyelin synthase 1 (SMS1)-knockdown T cells. Int. Immunol. 20:1427–1437.
  • Kolesnick RN, Haimovitz-Friedman A, Fuks Z. 1994. The sphingomyelin signal transduction pathway mediates apoptosis for tumor necrosis factor, Fas, and ionizing radiation. Biochem. Cell Biol. 72:471–474.
  • Kostenis E. 2004. Novel clusters of receptors for sphingosine-1-phosphate, sphingosylphosphorylcholine, and (lyso)-phosphatidic acid: new receptors for “old” ligands. J. Cell Biochem. 92:923–936.
  • Lagane B, et al. 2008. CXCR4 dimerization and beta-arrestin-mediated signaling account for the enhanced chemotaxis to CXCL12 in WHIM syndrome. Blood 112:34–44.
  • Li Z, et al. 2007. Inhibition of sphingomyelin synthase (SMS) affects intracellular sphingomyelin accumulation and plasma membrane lipid organization. Biochim. Biophys. Acta 1771:1186–1194.
  • Liang Z, et al. 2004. Inhibition of breast cancer metastasis by selective synthetic polypeptide against CXCR4. Cancer Res. 64:4302–4308.
  • Liang Z, et al. 2005. Silencing of CXCR4 blocks breast cancer metastasis. Cancer Res. 65:967–971.
  • Limatola C, et al. 2007. Evidence for a role of glycosphingolipids in CXCR4-dependent cell migration. FEBS Lett. 581:2641–2646.
  • Luberto C, Hannun YA. 1998. Sphingomyelin synthase, a potential regulator of intracellular levels of ceramide and diacylglycerol during SV40 transformation. Does sphingomyelin synthase account for the putative phosphatidylcholine-specific phospholipase C? J. Biol. Chem. 273:14550–14559.
  • Luster AD. 1998. Chemokines—chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 338:436–445.
  • Manes S, Ana Lacalle R, Gomez-Mouton C, Martinez AC. 2003. From rafts to crafts: membrane asymmetry in moving cells. Trends Immunol. 24:320–326.
  • Mitsutake S, et al. 2011. Dynamic modification of sphingomyelin in lipid microdomains controls development of obesity, Fatty liver, and type 2 diabetes. J. Biol. Chem. 286:28544–28555.
  • Mochizuki N, et al. 2001. Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411:1065–1068.
  • Muller A, et al. 2001. Involvement of chemokine receptors in breast cancer metastasis. Nature 410:50–56.
  • Nagasawa T, et al. 1996. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 382:635–638.
  • Ng GY, et al. 1996. Dopamine D2 receptor dimers and receptor-blocking peptides. Biochem. Biophys. Res. Commun. 227:200–204.
  • Nguyen DH, Taub D. 2002. CXCR4 function requires membrane cholesterol: implications for HIV infection. J. Immunol. 168:4121–4126.
  • Parton RG, Hancock JF. 2004. Lipid rafts and plasma membrane microorganization: insights from Ras. Trends Cell Biol. 14:141–147.
  • Percherancier Y, et al. 2005. Bioluminescence resonance energy transfer reveals ligand-induced conformational changes in CXCR4 homo- and heterodimers. J. Biol. Chem. 280:9895–9903.
  • Pettus BJ, Chalfant CE, Hannun YA. 2002. Ceramide in apoptosis: an overview and current perspectives. Biochim. Biophys. Acta 1585:114–125.
  • Ramsay D, Kellett E, McVey M, Rees S, Milligan G. 2002. Homo- and hetero-oligomeric interactions between G-protein-coupled receptors in living cells monitored by two variants of bioluminescence resonance energy transfer (BRET): hetero-oligomers between receptor subtypes form more efficiently than between less closely related sequences. Biochem. J. 365:429–440.
  • Riboni L, Viani P, Bassi R, Giussani P, Tettamanti G. 2001. Basic fibroblast growth factor-induced proliferation of primary astrocytes. evidence for the involvement of sphingomyelin biosynthesis. J. Biol. Chem. 276:12797–12804.
  • Romano C, Yang WL, O'Malley KL. 1996. Metabotropic glutamate receptor 5 is a disulfide-linked dimer. J. Biol. Chem. 271:28612–28616.
  • Separovic D, et al. 2007. Sphingomyelin synthase 1 suppresses ceramide production and apoptosis post-photodamage. Biochem. Biophys. Res. Commun. 358:196–202.
  • Separovic D, et al. 2008. Suppression of sphingomyelin synthase 1 by small interference RNA is associated with enhanced ceramide production and apoptosis after photodamage. Exp. Cell Res. 314:1860–1868.
  • Shakor AB, et al. 2011. Sphingomyelin synthase 1-generated sphingomyelin plays an important role in transferrin trafficking and cell proliferation. J. Biol. Chem. 286:36053–36062.
  • Sierro F, et al. 2007. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc. Natl. Acad. Sci. U. S. A. 104:14759–14764.
  • Silvius JR. 2003. Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim. Biophys. Acta 1610:174–183.
  • Simons K, Ikonen E. 1997. Functional rafts in cell membranes. Nature 387:569–572.
  • Simons K, Toomre D. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31–39.
  • Tachibana K, et al. 1998. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393:591–594.
  • Tafesse FG, et al. 2007. Both sphingomyelin synthases SMS1 and SMS2 are required for sphingomyelin homeostasis and growth in human HeLa cells. J. Biol. Chem. 282:17537–17547.
  • Tafesse FG, Ternes P, Holthuis JC. 2006. The multigenic sphingomyelin synthase family. J. Biol. Chem. 281:29421–29425.
  • Vila-Coro AJ, et al. 1999. The chemokine SDF-1α triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway. FASEB J. 13:1699–1710.
  • Wang G, Krishnamurthy K, Chiang YW, Dasgupta S, Bieberich E. 2008. Regulation of neural progenitor cell motility by ceramide and potential implications for mouse brain development. J. Neurochem. 106:718–733.
  • Wang J, He L, Combs CA, Roderiquez G, Norcross MA. 2006. Dimerization of CXCR4 in living malignant cells: control of cell migration by a synthetic peptide that reduces homologous CXCR4 interactions. Mol. Cancer Ther. 5:2474–2483.
  • Wiesner DA, Dawson G. 1996. Staurosporine induces programmed cell death in embryonic neurons and activation of the ceramide pathway. J. Neurochem. 66:1418–1425.
  • Yamaji-Hasegawa A, et al. 2003. Oligomerization and pore formation of a sphingomyelin-specific toxin, lysenin. J. Biol. Chem. 278:22762–22770.
  • Yamaoka S, Miyaji M, Kitano T, Umehara H, Okazaki T. 2004. Expression cloning of a human cDNA restoring sphingomyelin synthesis and cell growth in sphingomyelin synthase-defective lymphoid cells. J. Biol. Chem. 279:18688–18693.
  • Yano M, et al. 2011. Mitochondrial dysfunction and increased reactive oxygen species impair insulin secretion in sphingomyelin synthase 1-null mice. J. Biol. Chem. 286:3992–4002.
  • Yasumoto K, et al. 2006. Role of the CXCL12/CXCR4 axis in peritoneal carcinomatosis of gastric cancer. Cancer Res. 66:2181–2187.
  • Yeang C, et al. 2008. The domain responsible for sphingomyelin synthase (SMS) activity. Biochim. Biophys. Acta 1781:610–617.
  • Zeng FY, Wess J. 1999. Identification and molecular characterization of m3 muscarinic receptor dimers. J. Biol. Chem. 274:19487–19497.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.