Loss of the ceramide transfer protein augments EGF receptor signaling in breast cancer

Cancer Research

Volumn 72, Issue 11, 2012, Pages 2855-2866

  Heering, Johanna ^a   Weis, Nicole ^a   Holeiter, Monika ^a,f   Neugart, Felix ^a   Staebler, Annette ^b   Fehm, Tanja N ^b   Bischoff, Annabell ^a   Schiller, Jürgen ^c   Duss, Stephan ^d   Schmid, Simone ^a   Korte, Thomas ^e   Herrmann, Andreas ^e   Olayioye, Monilola A ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

^d FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^e HUMBOLDT UNIVERSITY   (Germany)

^f FRAUNHOFER INSTITUTE FOR INTERFACIAL ENGINEERING AND BIOTECHNOLOGY IGB   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CERAMIDE; CERAMIDE TRANSFER PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; LIGAND; PROTEIN CERT; SPHINGOMYELIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHOSPHORYLATION; CANCER CELL; CELL LEVEL; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERNALIZATION; INTRACELLULAR TRANSPORT; LIPID TRANSPORT; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER; UPREGULATION;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; FOCAL ADHESIONS; HUMANS; PHOSPHOLIPASE D; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84861881638     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-3069     Document Type: Article

References (46)

1. Di Cosimo S, Baselga J. Management of breast cancer with targeted agents: importance of heterogeneity. [corrected]. Nat Rev Clin Oncol 2010;7:139-47.
2. Hurvitz SA, Finn RS. What's positive about 'triple-negative' breast cancer? Future Oncol 2009;5:1015-25.
3. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001;2:127-37. (Pubitemid 33674041)
4. Hancock JF. Lipid rafts: contentious only from simplistic standpoints. Nat Rev Mol Cell Biol 2006;7:456-62. (Pubitemid 44050099)
5. Levental I, Grzybek M, Simons K. Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 2010;49:6305-16.
6. Miyaji M, Jin ZX, Yamaoka S, Amakawa R, Fukuhara S, Sato SB, et al. Role of membrane sphingomyelin and ceramide in platform formation for Fas-mediated apoptosis. J Exp Med 2005;202:249-59. (Pubitemid 41043821)
7. Jin ZX, Huang CR, Dong L, Goda S, Kawanami T, Sawaki T, et al. Impaired TCR signaling through dysfunction of lipid rafts in sphingomyelin synthase 1 (SMS1)-knockdown T cells. Int Immunol 2008; 20:1427-37.
8. Pike LJ. Growth factor receptors, lipid rafts and caveolae: an evolving story. Biochim Biophys Acta 2005;1746:260-73.
9. Clayton AH, Walker F, Orchard SG, Henderson C, Fuchs D, Rothacker J, et al. Ligand-induced dimer-tetramer transition during the activation of the cell surface epidermal growth factor receptor - a multidimensional microscopy analysis. J Biol Chem 2005;280:30392-9. (Pubitemid 41216222)
10. Saffarian S, Li Y, Elson EL, Pike LJ. Oligomerization of the EGFreceptor investigated by live cell fluorescence intensity distribution analysis. Biophys J 2007;93:1021-31. (Pubitemid 47219793)
11. Ariotti N, Liang H, Xu Y, Zhang Y, Yonekubo Y, Inder K, et al. Epidermal growth factor receptor activation remodels the plasma membrane lipid environment to induce nanocluster formation. Mol Cell Biol 2010;30: 3795-804.
12. Hanada K, Kumagai K, Yasuda S, Miura Y, Kawano M, Fukasawa M, et al. Molecular machinery for non-vesicular trafficking of ceramide. Nature 2003;426:803-9. (Pubitemid 38056858)
13. Fukasawa M, Nishijima M, Itabe H, Takano T, Hanada K. Reduction of sphingomyelin level without accumulation of ceramide in Chinese hamster ovary cells affects detergent-resistant membrane domains and enhances cellular cholesterol efflux to methyl-beta -cyclodextrin. J Biol Chem 2000;275:34028-34.
14. Wang X, Rao RP, Kosakowska-Cholody T, Masood MA, Southon E, Zhang H, et al. Mitochondrial degeneration and not apoptosis is the primary cause of embryonic lethality in ceramide transfer protein mutant mice. J Cell Biol 2009;184:143-58.
15. Rao RP, Yuan C, Allegood JC, Rawat SS, Edwards MB, Wang X, et al. Ceramide transfer protein function is essential for normal oxidative stress response and lifespan. Proc Natl Acad Sci U S A 2007; 104:11364-9. (Pubitemid 47175146)
16. Perry RJ, Ridgway ND. Molecular mechanisms and regulation of ceramide transport. Biochim Biophys Acta 2005;1734:220-34.
17. Hanada K, Kumagai K, Tomishige N, Yamaji T. CERT-mediated trafficking of ceramide. Biochim Biophys Acta 2009;1791:684-91.
18. Fuchs B, Schiller J, Suss R, Zscharnack M, Bader A, Müller P, et al. Analysis of stem cell lipids by offline HPTLC-MALDI-TOF MS. Anal Bioanal Chem 2008;392:849-60.
19. Farmer P, Bonnefoi H, Becette V, Tubiana-Hulin M, Fumoleau P, Larsimont D, et al. Identification of molecular apocrine breast tumours by microarray analysis. Oncogene 2005;24:4660-71. (Pubitemid 41032603)
20. Richardson AL, Wang ZC, De Nicolo A, Lu X, Brown M, Miron A, et al. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 2006;9:121-32. (Pubitemid 43202662)
21. Yamaji A, Sekizawa Y, Emoto K, Sakuraba H, Inoue K, Kobayashi H, et al. Lysenin, a novel sphingomyelin-specific binding protein. J Biol Chem 1998;273:5300-6. (Pubitemid 28108696)
22. Bozulic L, Hemmings BA. PIKKing on PKB: regulation of PKB activity by phosphorylation. Curr Opin Cell Biol 2009;21:256-61.
23. Huitema K, van den DJ, Brouwers JF, Holthuis JC. Identification of a family of animal sphingomyelin synthases. EMBO J 2004;23: 33-44. (Pubitemid 38165745)
24. Villani M, Subathra M, Im YB, Choi Y, Signorelli P, Del Poeta M, et al. Sphingomyelin synthases regulate production of diacylglycerol at the Golgi. Biochem J 2008;414:31-41.
25. Graus-Porta D, Beerli RR, Daly JM, Hynes NE. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 1997;16:1647-55. (Pubitemid 27151960)
26. Tzahar E, Waterman H, Chen X, Levkowitz G, Karunagaran D, Lavi S, et al. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol Cell Biol 1996;16:5276-87. (Pubitemid 26315047)
27. Pike LJ, Casey L. Cholesterol levels modulate EGF receptor-mediated signaling by altering receptor function and trafficking. Biochemistry 2002;41:10315-22. (Pubitemid 34856457)
28. Roepstorff K, Thomsen P, Sandvig K, van Deurs B. Sequestration of epidermal growth factor receptors in non-caveolar lipid rafts inhibits ligand binding. J Biol Chem 2002;277:18954-60. (Pubitemid 34959960)
29. Fugmann T, Hausser A, Schoffler P, Schmid S, Pfizenmaier K, Olayioye MA. Regulation of secretory transport by protein kinase D-mediated phosphorylation of the ceramide transfer protein. J Cell Biol 2007;178: 15-22. (Pubitemid 47026398)
30. Sorkin A, von Zastrow M. Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 2009;10:609-22.
31. Lee CS, Kim KL, Jang JH, Choi YS, Suh PG, Ryu SH. The roles of phospholipase D in EGFR signaling. Biochim Biophys Acta 2009;1791:862-8.
32. Jenkins GM, Frohman MA. Phospholipase D: a lipid centric review. Cell Mol Life Sci 2005;62:2305-16. (Pubitemid 41500546)
33. Shen Y, Xu L, Foster DA. Role for phospholipase D in receptor-mediated endocytosis. Mol Cell Biol 2001;21:595-602. (Pubitemid 32037377)
34. Zeidan YH, Hannun YA. Translational aspects of sphingolipid metabolism. Trends Mol Med 2007;13:327-36. (Pubitemid 47126985)
35. Swanton C, Marani M, Pardo O, Warne PH, Kelly G, Sahai E, et al. Regulators of mitotic arrest and ceramide metabolism are determinants of sensitivity to paclitaxel and other chemotherapeutic drugs. Cancer Cell 2007;11:498-512. (Pubitemid 46856907)
36. Kumagai K, Kawano M, Shinkai-Ouchi F, Nishijima M, Hanada K. Interorganelle trafficking of ceramide is regulated by phosphorylation- dependent cooperativity between the PH and START domains of CERT. J Biol Chem 2007;282:17758-66. (Pubitemid 47100308)
37. Perry RJ, Ridgway ND. Oxysterol-binding protein and vesicle-associated membrane protein-associated protein are required for steroldependent activation of the ceramide transport protein. Mol Biol Cell 2006;17:2604-16. (Pubitemid 43825498)
38. Noh DY, Ahn SJ, Lee RA, Park IA, Kim JH, Suh PG, et al. Overexpression of phospholipase D1 in human breast cancer tissues. Cancer Lett 2000;161:207-14.
39. Uchida N, Okamura S, Nagamachi Y, Yamashita S. Increased phospholipase D activity in human breast cancer. J Cancer Res Clin Oncol 1997;123:280-5. (Pubitemid 27230904)
40. Joseph T, Wooden R, Bryant A, Zhong M, Lu Z, Foster DA. Transformation of cells overexpressing a tyrosine kinase by phospholipase D1 and D2. Biochem Biophys Res Commun 2001;289: 1019-24. (Pubitemid 34076291)
41. Lu Z, Hornia A, Joseph T, Sukezane T, Frankel P, Zhong M, et al. Phospholipase D and RalA cooperate with the epidermal growth factor receptor to transform 3Y1 rat fibroblasts. Mol Cell Biol 2000; 20:462-7. (Pubitemid 30023087)
42. Zheng Y, Rodrik V, Toschi A, Shi M, Hui L, Shen Y, et al. Phospholipase D couples survival and migration signals in stress response of human cancer cells. J Biol Chem 2006;281:15862-8. (Pubitemid 43848477)
43. Donaldson JG. Phospholipase D in endocytosis and endosomal recycling pathways. Biochim Biophys Acta 2009;1791:845-9.
44. Su W, Chen Q, Frohman MA. Targeting phospholipase D with small-molecule inhibitors as a potential therapeutic approach for cancer metastasis. Future Oncol 2009;5:1477-86.
45. Sun T, Aceto N, Meerbrey KL, Kessler JD, Zhou C, Migliaccio I, et al. Activation of multiple proto-oncogenic tyrosine kinases in breast cancer via loss of the PTPN12 phosphatase. Cell 2011;144: 703-18.
46. Klein S, Levitzki A. Targeting the EGFRand the PKB pathway in cancer. Curr Opin Cell Biol 2009;21:185-93.