Integrative Analysis of Subcellular Quantitative Proteomics Studies Reveals Functional Cytoskeleton Membrane-Lipid Raft Interactions in Cancer

Journal of Proteome Research

Volumn 15, Issue 10, 2016, Pages 3451-3462

  Shah, Anup D ^a   Inder, Kerry L ^a   Shah, Alok K ^a   Cristino, Alexandre S ^a   McKie, Arthur B ^b   Gabra, Hani ^b   Davis, Melissa J ^c   Hill, Michelle M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

cancer progression; computational biology; cytoskeleton; lipid raft; quantitative proteomics

Indexed keywords

CAVIN 1 PROTEIN; CYTOSKELETON PROTEIN; MERLIN; OPCML PROTEIN; POLYMERASE I AND TRANSCRIPT RELEASE FACTOR; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; OPCML PROTEIN, HUMAN; PROTEOME;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER GROWTH; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; FEMALE; KIDNEY CARCINOMA; LIPID RAFT; MALE; MELANOMA; MICROFILAMENT; MODULATION; NEOPLASM; NONHUMAN; OVARIAN CANCER CELL LINE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; CELL MEMBRANE; CHEMISTRY; COMPUTER SIMULATION; DISEASE COURSE; HUMAN; MEMBRANE MICRODOMAIN; METABOLISM; OVARY TUMOR; PATHOLOGY; PROCEDURES; PROTEIN DOMAIN; TUMOR CELL LINE; ULTRASTRUCTURE;

CELL ADHESION MOLECULES; CELL LINE, TUMOR; CELL MEMBRANE; COMPUTER SIMULATION; CYTOSKELETON; DISEASE PROGRESSION; FEMALE; GPI-LINKED PROTEINS; HUMANS; MEMBRANE MICRODOMAINS; NEOPLASMS; OVARIAN NEOPLASMS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEOME; PROTEOMICS;

EID: 84990834226     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b01035     Document Type: Article

References (68)

1. Hanahan, D.; Weinberg, R. A. Hallmarks of cancer: the next generation Cell 2011, 144 (5) 646-674 10.1016/j.cell.2011.02.013
2. Gupta, G. P.; Massagué, J. Cancer metastasis: building a framework Cell 2006, 127 (4) 679-695 10.1016/j.cell.2006.11.001
3. Staubach, S.; Hanisch, F.-G. Lipid rafts: signaling and sorting platforms of cells and their roles in cancer Expert Rev. Proteomics 2011, 8 (2) 263-277 10.1586/epr.11.2
4. Irwin, M. E.; Mueller, K. L.; Bohin, N.; Ge, Y.; Boerner, J. L. Lipid raft localization of EGFR alters the response of cancer cells to the EGFR tyrosine kinase inhibitor gefitinib J. Cell. Physiol. 2011, 226 (9) 2316-2328 10.1002/jcp.22570
5. Chinni, S. R.; Yamamoto, H.; Dong, Z.; Sabbota, A.; Bonfil, R. D.; Cher, M. L. CXCL12/CXCR4 transactivates HER2 in lipid rafts of prostate cancer cells and promotes growth of metastatic deposits in bone Mol. Cancer Res. 2008, 6 (3) 446-457 10.1158/1541-7786.MCR-07-0117
6. Casaletto, J. B.; McClatchey, A. I. Spatial regulation of receptor tyrosine kinases in development and cancer Nat. Rev. Cancer 2012, 12 (6) 387-400 10.1038/nrc3277
7. Freeman, M. R.; Cinar, B.; Lu, M. L. Membrane rafts as potential sites of nongenomic hormonal signaling in prostate cancer Trends Endocrinol. Metab. 2005, 16 (6) 273-279 10.1016/j.tem.2005.06.002
8. Babina, I. S.; Donatello, S.; Nabi, I. R.; Hopkins, A. M. Lipid Rafts As Master Regulators of Breast Cancer Cell Function,. http://epubs.rcsi.ie/surgart.
9. 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. 2006, 281 (26) 18145-18155 10.1074/jbc.M512566200
10. Delmas, D.; Rébé, C.; Lacour, S.; Filomenko, R.; Athias, A.; Gambert, P.; Cherkaoui-Malki, M.; Jannin, B.; Dubrez-Daloz, L.; Latruffe, N. Resveratrol-induced apoptosis is associated with Fas redistribution in the rafts and the formation of a death-inducing signaling complex in colon cancer cells J. Biol. Chem. 2003, 278 (42) 41482-41490 10.1074/jbc.M304896200
11. Caruso, J. A.; Stemmer, P. M. Proteomic profiling of lipid rafts in a human breast cancer model of tumorigenic progression Clin. Exp. Metastasis 2011, 28 (6) 529-540 10.1007/s10585-011-9389-5
12. Baruthio, F.; Quadroni, M.; Rüegg, C.; Mariotti, A. Proteomic analysis of membrane rafts of melanoma cells identifies protein patterns characteristic of the tumor progression stage Proteomics 2008, 8 (22) 4733-4747 10.1002/pmic.200800169
13. Raimondo, F.; Corbetta, S.; Savoia, A.; Chinello, C.; Cazzaniga, M.; Rocco, F.; Bosari, S.; Grasso, M.; Bovo, G.; Magni, F.; Pitto, M. Comparative membrane proteomics: a technical advancement in the search of renal cell carcinoma biomarkers Mol. BioSyst. 2015, 11 (6) 1708-1716 10.1039/C5MB00020C
14. Inder, K. L.; Zheng, Y. Z.; Davis, M. J.; Moon, H.; Loo, D.; Nguyen, H.; Clements, J. A.; Parton, R. G.; Foster, L. J.; Hill, M. M. Expression of PTRF in PC-3 cells modulates cholesterol dynamics and the actin cytoskeleton impacting secretion pathways Mol. Cell. Proteomics 2012, 11 (2) M111. 012245 10.1074/mcp.M111.012245
15. Moon, H.; Lee, C.; Inder, K.; Sharma, S.; Choi, E.; Black, D.; Le Cao, K.; Winterford, C.; Coward, J.; Ling, M. et al. PTRF/cavin-1 neutralizes non-caveolar caveolin-1 microdomains in prostate cancer Oncogene 2014, 33 (27) 3561-3570 10.1038/onc.2013.315
16. Stickney, J. T.; Bacon, W. C.; Rojas, M.; Ratner, N.; Ip, W. Activation of the tumor suppressor merlin modulates its interaction with lipid rafts Cancer Res. 2004, 64 (8) 2717-2724 10.1158/0008-5472.CAN-03-3798
17. Ntougkos, E.; Rush, R.; Scott, D.; Frankenberg, T.; Gabra, H.; Smyth, J. F.; Sellar, G. C. The IgLON family in epithelial ovarian cancer: expression profiles and clinicopathologic correlates Clin. Cancer Res. 2005, 11 (16) 5764-5768 10.1158/1078-0432.CCR-04-2388
18. Sellar, G. C.; Watt, K. P.; Rabiasz, G. J.; Stronach, E. A.; Li, L.; Miller, E. P.; Massie, C. E.; Miller, J.; Contreras-Moreira, B.; Scott, D. et al. OPCML at 11q25 is epigenetically inactivated and has tumor-suppressor function in epithelial ovarian cancer Nat. Genet. 2003, 34 (3) 337-343 10.1038/ng1183
19. The Cancer Genome Atlas Research Network Integrated genomic analyses of ovarian carcinoma Nature 2011, 474 (7353) 609-615 10.1038/nature10166
20. McKie, A. B.; Vaughan, S.; Zanini, E.; Okon, I. S.; Louis, L.; de Sousa, C.; Greene, M. I.; Wang, Q.; Agarwal, R.; Shaposhnikov, D. et al. The OPCML tumor suppressor Functions as a cell surface repressor-adaptor, Negatively regulating receptor tyrosine Kinases in epithelial Ovarian cancer Cancer Discovery 2012, 2 (2) 156-171 10.1158/2159-8290.CD-11-0256
21. Zhou, F.; Tao, G.; Chen, X.; Xie, W.; Liu, M.; Cao, X. Methylation of OPCML promoter in ovarian cancer tissues predicts poor patient survival Clin. Chem. Lab. Med. 2014, 52 (5) 735-742 10.1515/cclm-2013-0736
22. Wu, S. Y.; Sood, A. K. New roles opined for OPCML Cancer Discovery 2012, 2 (2) 115-116 10.1158/2159-8290.CD-11-0356
23. Shah, A.; Chen, D.; Boda, A. R.; Foster, L. J.; Davis, M. J.; Hill, M. M. RaftProt: mammalian lipid raft proteome database Nucleic Acids Res. 2015, 43 (D1) D335-D338 10.1093/nar/gku1131
24. Carbon, S.; Ireland, A.; Mungall, C. J.; Shu, S.; Marshall, B.; Lewis, S. AmiGO: online access to ontology and annotation data Bioinformatics 2009, 25 (2) 288-289 10.1093/bioinformatics/btn615
25. Moon, H.; Ruelcke, J. E.; Choi, E.; Sharpe, L. J.; Nassar, Z. D.; Bielefeldt-Ohmann, H.; Parat, M.-O.; Shah, A.; Francois, M.; Inder, K. L. et al. Diet-induced hypercholesterolemia promotes androgen-independent prostate cancer metastasis via IQGAP1 and caveolin-1 Oncotarget 2015, 6 (10) 7438-7453 10.18632/oncotarget.3476
26. Inder, K. L.; Loo, D.; Zheng, Y. Z.; Parton, R. G.; Foster, L. J.; Hill, M. Normalization of protein at different stages in SILAC subcellular proteomics affects functional analysis J. Integr. OMICS 2012, 2 (2) 114-122 10.5584/jiomics.v2i2.108
27. Zheng, Y. Z.; Boscher, C.; Inder, K. L.; Fairbank, M.; Loo, D.; Hill, M. M.; Nabi, I. R.; Foster, L. J. Differential impact of caveolae and caveolin-1 scaffolds on the membrane raft proteome Mol. Cell. Proteomics 2011, 10 (10) M110.007146 10.1074/mcp.M110.007146
28. Foster, L. J.; de Hoog, C. L.; Mann, M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors Proc. Natl. Acad. Sci. U. S. A. 2003, 100 (10) 5813-5818 10.1073/pnas.0631608100
29. Lingwood, D.; Simons, K. Detergent resistance as a tool in membrane research Nat. Protoc. 2007, 2 (9) 2159-2165 10.1038/nprot.2007.294
30. Pike, L. J.; Han, X.; Chung, K.-N.; Gross, R. W. Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis Biochemistry 2002, 41 (6) 2075-2088 10.1021/bi0156557
31. The Common Repository of Adventitious Proteins (cRAP) Database. ftp://ftp.thegpm.org/fasta/cRAP (accessed Aug 18, 2014).
32. Chen, D.; Shah, A.; Nguyen, H.; Loo, D.; Inder, K. L.; Hill, M. M. Online quantitative proteomics p-value calculator for permutation-based statistical testing of peptide ratios J. Proteome Res. 2014, 13 (9) 4184-4191 10.1021/pr500525e
33. Nguyen, H. D.; Wood, I.; Hill, M. M. A robust permutation test for quantitative SILAC proteomics experiments J. Integr. OMICS 2012, 2 (2) 80-93 10.5584/jiomics.v2i2.109
34. Cowley, M. J.; Pinese, M.; Kassahn, K. S.; Waddell, N.; Pearson, J. V.; Grimmond, S. M.; Biankin, A. V.; Hautaniemi, S.; Wu, J. PINA v2. 0: mining interactome modules Nucleic Acids Res. 2012, 40, D862-D865 10.1093/nar/gkr967
35. Prasad, T. K.; Goel, R.; Kandasamy, K.; Keerthikumar, S.; Kumar, S.; Mathivanan, S.; Telikicherla, D.; Raju, R.; Shafreen, B.; Venugopal, A. et al. Human protein reference database-2009 update Nucleic Acids Res. 2009, 37 (suppl 1) D767-D772 10.1093/nar/gkn892
36. Kerrien, S.; Aranda, B.; Breuza, L.; Bridge, A.; Broackes-Carter, F.; Chen, C.; Duesbury, M.; Dumousseau, M.; Feuermann, M.; Hinz, U. et al. The IntAct molecular interaction database in 2012 Nucleic Acids Res. 2012, 40, D841-D846 10.1093/nar/gkr1088
37. Chatr-aryamontri, A.; Breitkreutz, B.-J.; Oughtred, R.; Boucher, L.; Heinicke, S.; Chen, D.; Stark, C.; Breitkreutz, A.; Kolas, N.; O'Donnell, L. et al. The BioGRID interaction database: 2015 update Nucleic Acids Res. 2015, 43, D470-D478 10.1093/nar/gku1204
38. Licata, L.; Briganti, L.; Peluso, D.; Perfetto, L.; Iannuccelli, M.; Galeota, E.; Sacco, F.; Palma, A.; Nardozza, A. P.; Santonico, E. et al. MINT, the molecular interaction database: 2012 update Nucleic Acids Res. 2012, 40 (D1) D857-D861 10.1093/nar/gkr930
39. Salwinski, L.; Miller, C. S.; Smith, A. J.; Pettit, F. K.; Bowie, J. U.; Eisenberg, D. The database of interacting proteins: 2004 update Nucleic Acids Res. 2004, 32 (suppl 1) D449-D451 10.1093/nar/gkh086
40. Güldener, U.; Münsterkötter, M.; Oesterheld, M.; Pagel, P.; Ruepp, A.; Mewes, H.-W.; Stümpflen, V. MPact: the MIPS protein interaction resource on yeast Nucleic Acids Res. 2006, 34 (suppl 1) D436-D441 10.1093/nar/gkj003
41. Cline, M. S.; Smoot, M.; Cerami, E.; Kuchinsky, A.; Landys, N.; Workman, C.; Christmas, R.; Avila-Campilo, I.; Creech, M.; Gross, B. et al. Integration of biological networks and gene expression data using Cytoscape Nat. Protoc. 2007, 2 (10) 2366-2382 10.1038/nprot.2007.324
42. Csardi, G.; Nepusz, T. The igraph software package for complex network research InterJournal, Complex Systems 2006, 1695 (5) 1-9
43. Zhou, Y.; Liang, H.; Rodkey, T.; Ariotti, N.; Parton, R. G.; Hancock, J. F. Signal integration by lipid-mediated spatial cross talk between Ras nanoclusters Mol. Cell. Biol. 2014, 34 (5) 862-876 10.1128/MCB.01227-13
44. Mueller, V.; Ringemann, C.; Honigmann, A.; Schwarzmann, G.; Medda, R.; Leutenegger, M.; Polyakova, S.; Belov, V.; Hell, S.; Eggeling, C. STED nanoscopy reveals molecular details of cholesterol-and cytoskeleton-modulated lipid interactions in living cells Biophys. J. 2011, 101 (7) 1651-1660 10.1016/j.bpj.2011.09.006
45. Gómez-Llobregat, J.; Buceta, J.; Reigada, R. Interplay of cytoskeletal activity and lipid phase stability in dynamic protein recruitment and clustering Sci. Rep. 2013, 3, 2608 10.1038/srep02608
46. Wickström, S. A.; Alitalo, K.; Keski-Oja, J. Endostatin associates with lipid rafts and induces reorganization of the actin cytoskeleton via down-regulation of RhoA activity J. Biol. Chem. 2003, 278 (39) 37895-37901 10.1074/jbc.M303569200
47. Head, B. P.; Patel, H. H.; Insel, P. A. Interaction of membrane/lipid rafts with the cytoskeleton: impact on signaling and function: membrane/lipid rafts, mediators of cytoskeletal arrangement and cell signaling Biochim. Biophys. Acta, Biomembr. 2014, 1838 (2) 532-545 10.1016/j.bbamem.2013.07.018
48. Li, Y.; Kang, Y. S.; Dai, C.; Kiss, L. P.; Wen, X.; Liu, Y. Epithelial-to-mesenchymal transition is a potential pathway leading to podocyte dysfunction and proteinuria Am. J. Pathol. 2008, 172 (2) 299-308 10.2353/ajpath.2008.070057
49. Kalluri, R.; Weinberg, R. A. The basics of epithelial-mesenchymal transition J. Clin. Invest. 2009, 119 (6) 1420-1428 10.1172/JCI39104
50. Schlegel, N.; Meir, M.; Heupel, W.-M.; Holthöfer, B.; Leube, R. E.; Waschke, J. Desmoglein 2-mediated adhesion is required for intestinal epithelial barrier integrity Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298 (5) G774-G783 10.1152/ajpgi.00239.2009
51. Nicolau, D. V.; Burrage, K.; Parton, R. G.; Hancock, J. F. Identifying optimal lipid raft characteristics required to promote nanoscale protein-protein interactions on the plasma membrane Mol. Cell. Biol. 2006, 26 (1) 313-323 10.1128/MCB.26.1.313-323.2006
52. Byrum, J. N.; Rodgers, W. Membrane-cytoskeleton interactions in cholesterol-dependent domain formation Essays Biochem. 2015, 57, 177-187 10.1042/bse0570177
53. Türkcan, S.; Richly, M. U.; Alexandrou, A.; Masson, J.-B. Probing membrane protein interactions with their lipid raft environment using single-molecule tracking and Bayesian inference analysis PLoS One 2013, 8 (1) e53073 10.1371/journal.pone.0053073
54. Fife, C.; McCarroll, J.; Kavallaris, M. Movers and shakers: cell cytoskeleton in cancer metastasis Br. J. Pharmacol. 2014, 171 (24) 5507-5523 10.1111/bph.12704
55. Chichili, G. R.; Rodgers, W. Cytoskeleton-membrane interactions in membrane raft structure Cell. Mol. Life Sci. 2009, 66 (14) 2319-2328 10.1007/s00018-009-0022-6
56. Nicolson, G. L. Cell Membrane Fluid-Mosaic Structure and Cancer Metastasis Cancer Res. 2015, 75 (7) 1169-1176 10.1158/0008-5472.CAN-14-3216
57. Viola, A.; Gupta, N. Tether and trap: regulation of membrane-raft dynamics by actin-binding proteins Nat. Rev. Immunol. 2007, 7 (11) 889-896 10.1038/nri2193
58. McClatchey, A. I.; Giovannini, M. Membrane organization and tumorigenesis-the NF2 tumor suppressor, Merlin Genes Dev. 2005, 19 (19) 2265-2277 10.1101/gad.1335605
59. Vuoriluoto, K.; Haugen, H.; Kiviluoto, S.; Mpindi, J.; Nevo, J.; Gjerdrum, C.; Tiron, C.; Lorens, J.; Ivaska, J. Vimentin regulates EMT induction by Slug and oncogenic H-Ras and migration by governing Axl expression in breast cancer Oncogene 2011, 30 (12) 1436-1448 10.1038/onc.2010.509
60. Davidson, B.; Holth, A.; Hellesylt, E.; Tan, T. Z.; Huang, R. Y.-J.; Tropé, C.; Nesland, J. M.; Thiery, J. P. The clinical role of epithelial-mesenchymal transition and stem cell markers in advanced-stage ovarian serous carcinoma effusions Hum. Pathol. 2015, 46 (1) 1-8 10.1016/j.humpath.2014.10.004
61. Yi, B.-R.; Kim, T.-H.; Kim, Y.-S.; Choi, K.-C. Alteration of epithelial-mesenchymal transition markers in human normal ovaries and neoplastic ovarian cancers Int. J. Oncol. 2014, 46 (1) 272-280 10.3892/ijo.2014.2695
62. Li, C.; Tang, L.; Zhao, L.; Li, L.; Xiao, Q.; Luo, X.; Peng, W.; Ren, G.; Tao, Q.; Xiang, T. OPCML is frequently methylated in human colorectal cancer and its restored expression reverses EMT via downregulation of smad signaling Am. J. Cancer Res. 2015, 5 (5) 1635-1648
63. Lazo, P. A. Functional implications of tetraspanin proteins in cancer biology Cancer Sci. 2007, 98 (11) 1666-1677 10.1111/j.1349-7006.2007.00584.x
64. Ritter, L. M.; Boesze-Battaglia, K.; Tam, B. M.; Moritz, O. L.; Khattree, N.; Chen, S.-C.; Goldberg, A. F. Uncoupling of Photoreceptor Peripherin/rds Fusogenic Activity from Biosynthesis, Subunit Assembly, and Targeting a Potential Mechnism for Pathogenic Effects J. Biol. Chem. 2004, 279 (38) 39958-39967 10.1074/jbc.M403943200
65. Lee, E. S.; Burnside, B.; Flannery, J. G. Characterization of peripherin/rds and rom-1 transport in rod photoreceptors of transgenic and knockout animals Invest. Ophthalmol. Visual Sci. 2006, 47 (5) 2150-2160 10.1167/iovs.05-0919
66. Uhlén, M.; Fagerberg, L.; Hallström, B. M.; Lindskog, C.; Oksvold, P.; Mardinoglu, A.; Sivertsson, Å.; Kampf, C.; Sjöstedt, E.; Asplund, A. et al. Tissue-based map of the human proteome Science 2015, 347 (6220) 1260419 10.1126/science.1260419
67. Orädd, G.; Shahedi, V.; Lindblom, G. Effect of sterol structure on the bending rigidity of lipid membranes: A 2 H NMR transverse relaxation study Biochim. Biophys. Acta, Biomembr. 2009, 1788 (9) 1762-1771 10.1016/j.bbamem.2009.06.019
68. Kusumi, A.; Nakada, C.; Ritchie, K.; Murase, K.; Suzuki, K.; Murakoshi, H.; Kasai, R. S.; Kondo, J.; Fujiwara, T. Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules Annu. Rev. Biophys. Biomol. Struct. 2005, 34, 351-378 10.1146/annurev.biophys.34.040204.144637