Unsupervised Clustering of Subcellular Protein Expression Patterns in High-Throughput Microscopy Images Reveals Protein Complexes and Functional Relationships between Proteins

PLoS Computational Biology

Volumn 9, Issue 6, 2013, Pages

  Handfield, Louis François ^a   Chong, Yolanda T ^b   Simmons, Jibril ^a   Andrews, Brenda J ^b   Moses, Alan M ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CLUSTER ANALYSIS; CYTOLOGY; FLUORESCENCE; FLUORESCENCE MICROSCOPY; SUPERVISED LEARNING; THROUGHPUT;

COMPLEX RELATIONSHIPS; FUNCTIONAL RELATIONSHIP; HIGH RESOLUTION; HIGH-THROUGHPUT; MICROSCOPY IMAGES; PROTEIN COMPLEXES; PROTEIN EXPRESSION PATTERNS; SUB-CELLULAR; SUBCELLULAR LOCALIZATIONS; UNSUPERVISED CLUSTERING;

PROTEINS;

ARTICLE; CELL ORGANELLE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CLUSTER ANALYSIS; COMPLEX FORMATION; FLUORESCENCE ANALYSIS; FUNGUS GROWTH; HIGH THROUGHPUT MICROSCOPY; IMAGE ANALYSIS; MICROSCOPY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; YEAST CELL;

SACCHAROMYCETALES;

EID: 84879542641     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003085     Document Type: Article

References (62)

1. Glory E, Murphy R, (2007) Automated subcellular location determination and high-throughput microscopy. Developmental cell 12: 7-16.
2. Hamilton N, Pantelic R, Hanson K, Teasdale R, (2007) Fast automated cell phenotype image classification. BMC bioinformatics 8: 110.
3. Shamir L, Delaney J, Orlov N, Eckley D, Goldberg I, (2010) Pattern recognition software and techniques for biological image analysis. PLoS Computational Biology 6: e1000974.
4. Eisen M, Spellman P, Brown P, Botstein D, (1998) Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences 95: 14863.
5. Spellman P, Sherlock G, Zhang M, Iyer V, Anders K, et al. (1998) Comprehensive identification of cell cycle-regulated genes of the yeast saccharomyces cerevisiae by microarray hybridization. Molecular biology of the cell 9: 3273-3297.
6. Peng H, Long F, Zhou J, Leung G, Eisen M, et al. (2007) Automatic image analysis for gene expression patterns of y embryos. BMC Cell Biology 8: S7.
7. Tomancak P, Berman B, Beaton A, Weiszmann R, Kwan E, et al. (2007) Global analysis of patterns of gene expression during drosophila embryogenesis. Genome biology 8: R145.
8. Asur S, Ucar D, Parthasarathy S, (2007) An ensemble framework for clustering protein-protein interaction networks. Bioinformatics 23: i29-i40.
9. Chen X, Velliste M, Weinstein S, Jarvik J, Murphy R, (2003) Location proteomics-building sub-cellular location trees from high resolution 3 d fluorescence microscope images of randomly-tagged proteins. Proc sPie 4962: 298-306.
10. Chen X, Murphy RF, (2005) Objective clustering of proteins based on subcellular location patterns. Journal of Biomedicine and Biotechnology 2: 87.
11. Hamilton N, Teasdale R, (2008) Visualizing and clustering high throughput sub-cellular localization imaging. BMC bioinformatics 9: 81.
12. Cohen A, Geva-Zatorsky N, Eden E, Frenkel-Morgenstern M, Issaeva I, et al. (2008) Dynamic proteomics of individual cancer cells in response to a drug. Science 322: 1511-1516.
13. Farkash-Amar S, Eden E, Cohen A, Geva-Zatorsky N, Cohen L, et al. (2012) Dynamic proteomics of human protein level and localization across the cell cycle. PloS one 7: e48722.
14. Huh W, Falvo J, Gerke L, Carroll A, Howson R, et al. (2003) Global analysis of protein localization in budding yeast. Nature 425: 686-691.
15. Boland M, Markey M, Murphy R, (1998) Automated recognition of patterns characteristic of subcellular structures in fluorescence microscopy images. Cytometry 33: 366-375.
16. Chen S, Zhao T, Gordon G, Murphy R, (2007) Automated image analysis of protein localization in budding yeast. Bioinformatics 23: i66-i71.
17. Sigal A, Milo R, Cohen A, Geva-Zatorsky N, Klein Y, et al. (2006) Dynamic proteomics in individual human cells uncovers widespread cell-cycle dependence of nuclear proteins. Nature Methods 3: 525-531.
18. Buck T, Rao A, Coelho L, Fuhrman M, Jarvik J, et al. (2009) Cell cycle dependence of protein subcellular location inferred from static, asynchronous images. In: Engineering in Medicine and Biology Society, 2009. EMBC 2009. Annual International Conference of the IEEE. IEEE, pp. 1016-1019.
19. De Carvalho M, Lotufo R, Couprie M, (2007) Morphological segmentation of yeast by image anal-ysis. Image and Vision Computing 25: 34-39.
20. Ohya Y, Sese J, Yukawa M, Sano F, Nakatani Y, et al. (2005) High-dimensional and large-scale phenotyping of yeast mutants. Proceedings of the National Academy of Sciences of the United States of America 102: 19015.
21. Huh S, Lee D, Murphy R, (2009) Efficient framework for automated classification of subcellular patterns in budding yeast. Cytometry Part A 75: 934-940.
22. Nanni L, Lumini A, (2008) A reliable method for cell phenotype image classification. Artificial intelligence in medicine 43: 87-97.
23. Tong A, Lesage G, Bader G, Ding H, Xu H, et al. (2004) Global mapping of the yeast genetic interaction network. Science 303: 808-813.
24. Bengtsson E, Wahlby C, Lindblad J, (2004) Robust cell image segmentation methods. Pattern Recognition and Image Analysis 14: 157-167.
25. Saito T, Ohtani M, Sawai H, Sano F, Saka A, et al. (2004) Scmd: Saccharomyces cerevisiae morphological database. Nucleic acids research 32: D319-D322.
26. Newman J, Ghaemmaghami S, Ihmels J, Breslow D, Noble M, et al. (2006) Single-cell proteomic analysis of s. cerevisiae reveals the architecture of biological noise. Nature 441: 840-846.
27. Bar-Even A, Paulsson J, Maheshri N, Carmi M, O'Shea E, et al. (2006) Noise in protein expression scales with natural protein abundance. Nature genetics 38: 636-643.
28. Murphy R, Velliste M, Porreca G, (2003) Robust numerical features for description and classification of subcellular location patterns in fluorescence microscope images. The Journal of VLSI Signal Processing 35: 311-321.
29. Loader C (1999) Local regression and likelihood. Springer Verlag.
30. Efron B, Efron B (1982) The jackknife, the bootstrap, and other resampling plans, volume 38. SIAM. 92 p.
31. Drury L, Perkins G, Diffley J, (1997) The cdc4/34/53 pathway targets cdc6p for proteolysis in budding yeast. The EMBO journal 16: 5966-5976.
32. Verma R, Feldman R, Deshaies R, (1997) Sic1 is ubiquitinated in vitro by a pathway that requires cdc4, cdc34, and cyclin/cdk activities. Molecular biology of the cell 8: 1427.
33. Liu Q, Larsen B, Ricicova M, Orlicky S, Tekotte H, et al. (2011) Scfcdc4 enables mating type switching in yeast by cyclin-dependent kinase-mediated elimination of the ash1 transcriptional repressor. Molecular and Cellular Biology 31: 584-598.
34. Krek W, (1998) Proteolysis and the g1-s transition: the scf connection. Current opinion in genetics & development 8: 36-42.
35. Nguyen V, Co C, Irie K, Li J, (2000) Clb/cdc28 kinases promote nuclear export of the replication initiator proteins mcm2-7. Current Biology 10: 195-205.
36. Costanzo M, Nishikawa J, Tang X, Millman J, Schub O, et al. (2004) Cdk activity antagonizes whi5, an inhibitor of g1/s transcription in yeast. Cell 117: 899-913.
37. Kannan A, Ostendorf M, Rohlicek J, (1994) Maximum likelihood clustering of gaussians for speech recognition. Speech and Audio Processing, IEEE Transactions on 2: 453-455.
38. Saldanha A, (2004) Java treeviewextensible visualization of microarray data. Bioinformatics 20: 3246-3248.
39. Ashburner M, Ball C, Blake J, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. Nature genetics 25: 25.
40. Preuss D, Mulholland J, Kaiser C, Orlean P, Albright C, et al. (1991) Structure of the yeast endoplasmic reticulum: localization of er proteins using immunofluorescence and immunoelectron microscopy. Yeast (Chichester, England) 7: 891-911.
41. Sagot I, Klee S, Pellman D, (2001) Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nature cell biology 4: 42-50.
42. Drubin D, Nelson W, (1996) Origins of cell polarity. Cell 84: 335-344.
43. Dahlberg J, Lund E, Goodwin E, (2003) Nuclear translation: What is the evidence? Rna 9: 1-8.
44. Lorberg A, Schmitz H, Jacoby J, Heinisch J, (2001) Lrg1p functions as a putative gtpase-activating protein in the pkc1p-mediated cell integrity pathway in saccharomyces cerevisiae. Molecular Genetics and Genomics 266: 514-526.
45. Cherry J, Adler C, Ball C, Chervitz S, Dwight S, et al. (1998) Sgd: Saccharomyces genome database. Nucleic acids research 26: 73-79.
46. Krause S, Xu H, Gray J, (2008) The synthetic genetic network around pkc1 identifies novel modulators and components of protein kinase c signaling in saccharomyces cerevisiae. Eukaryotic cell 7: 1880-1887.
47. Bi E, Chiavetta J, Chen H, Chen G, Chan C, et al. (2000) Identification of novel, evolutionarily conserved cdc42p-interacting proteins and of redundant pathways linking cdc24p and cdc42p to actin polarization in yeast. Molecular biology of the cell 11: 773-793.
48. Yoshida S, Ichihashi R, Toh-e A, (2003) Ras recruits mitotic exit regulator lte1 to the bud cortex in budding yeast. The Journal of cell biology 161: 889-897.
49. Rossio V, Yoshida S, (2011) Spatial regulation of cdc55-pp2a by zds1/zds2 controls mitotic entry and mitotic exit in budding yeast. The Journal of cell biology 193: 445-454.
50. Freifelder D, (1960) Bud position in saccharomyces cerevisiae. Journal of bacteriology 80: 567.
51. Bairoch A (2008) Uniprotkb/swiss-prot: New and future developments. In: Data Integration in the Life Sciences. Springer. pp. 204-206.
52. Zhao T, Velliste M, Boland M, Murphy R, (2005) Object type recognition for automated analysis of protein subcellular location. Image Processing, IEEE Transactions on 14: 1351-1359.
53. Shaner N, Campbell R, Steinbach P, Giepmans B, Palmer A, et al. (2004) Improved monomeric red, orange and yellow uorescent proteins derived from discosoma sp. red uorescent protein. Nature biotechnology 22: 1567-1572.
54. Breit H, Rigoll G (2001) Improved person tracking using a combined pseudo-2d-HMM and Kalman filter approach with automatic background state adaptation. In: Image Processing, 2001. Proceedings. 2001 International Conference on. IEEE, volume 2, pp. 53-56.
55. Gander W, Golub G, Strebel R, (1994) Least-squares fitting of circles and ellipses. BIT Numerical Mathematics 34: 558-578.
56. Holland P, Welsch R, (1977) Robust regression using iteratively reweighted least-squares. Communications in Statistics-Theory and Methods 6: 813-827.
57. Hill P, Canagarajah C, Bull D, (2003) Image segmentation using a texture gradient based watershed transform. Image Processing, IEEE Transactions on 12: 1618-1633.
58. Barnard R, Pearce K, Schovanec L, (2001) Inequalities for the perimeter of an ellipse. Journal of mathematical analysis and applications 260: 295-306.
59. MacKay D (2003) Information theory, inference, and learning algorithms. Cambridge University Press.
60. Carpenter A, Jones T, Lamprecht M, Clarke C, Kang I, et al. (2006) Cellprofiler: image analysis software for identifying and quantifying cell phenotypes. Genome biology 7: R100.
61. Chen S, Zhao T, Gordon G, Murphy R (2006) A novel graphical model approach to segmenting cell images. In: Computational Intelligence and Bioinformatics and Computational Biology, 2006. CIBCB'06. 2006 IEEE Symposium on. IEEE, pp. 1-8.
62. Jepson A, Fleet D, (2010) Robust estimation. Lecture Notes for CSC 2503.