Proteomic profiling of secretome and adherent plasma membranes from distinct mammary epithelial cell subpopulations

Proteomics

Volumn 11, Issue 20, 2011, Pages 4029-4039

  Ji, Hong ^a,b   Goode, Robert J A ^a   Vaillant, Francois ^c,d   Mathivanan, Suresh ^a,b   Kapp, Eugene A ^a   Mathias, Rommel A ^a,b   Lindeman, Geoffrey J ^c,d   Visvader, Jane E ^c,d   Simpson, Richard J ^a,b  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

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

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Cell biology; Mammary stem cell niche; Plasma membrane; Secretome; Wnt10a

Indexed keywords

ALPHA6BETA4 INTEGRIN; EPHRIN B2; EPHRIN RECEPTOR A1; EPHRIN RECEPTOR A2; VERY LATE ACTIVATION ANTIGEN 2;

ANIMAL CELL; ARTICLE; BASAL STEM CELL; BREAST CELL; BREAST EPITHELIUM; CELL MEMBRANE; CELL POPULATION; GEL CHROMATOGRAPHY; LUMINAL PROGENITOR CELL; MAMMARY STEM CELL; MATURE LUMINAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; STEM CELL; TANDEM MASS SPECTROMETRY;

ANIMALS; CELL LINE; CELL MEMBRANE; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; MAMMARY GLANDS, ANIMAL; MICE; PROTEOMICS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 80053973210     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201100102     Document Type: Article

References (70)

1. Jones, D. L., Wagers, A. J., No place like home: anatomy and function of the stem cell niche. Nat. Rev. Mol. Cell Biol. 2008, 9, 11-21.
2. Polyak, K., Kalluri, R., The role of the microenvironment in mammary gland development and cancer. Cold Spring Harb. Perspect. Biol. 2010, 2, a003244.
3. Morrison, S. J., Spradling, A. C., Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008, 132, 598-611.
4. Mohyeldin, A., Garzon-Muvdi, T., Quinones-Hinojosa, A., Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 2010, 7, 150-161.
5. Marthiens, V., Kazanis, I., Moss, L., Long, K., Ffrench-Constant, C., Adhesion molecules in the stem cell niche - more than just staying in shape? J. Cell Sci. 2010, 123, 1613-1622.
6. Visvader, J. E., Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev. 2009, 23, 2563-2577.
7. Booth, B. W., Mack, D. L., Androutsellis-Theotokis, A., McKay, R. D. et al., The mammary microenvironment alters the differentiation repertoire of neural stem cells. Proc. Natl. Acad. Sci. USA 2008, 105, 14891-14896.
8. Ting, C. N., Olson, M. C., Barton, K. P., Leiden, J. M., Transcription factor GATA-3 is required for development of the T-cell lineage. Nature 1996, 384, 474-478.
9. Pai, S. Y., Truitt, M. L., Ting, C. N., Leiden, J. M. et al., Critical roles for transcription factor GATA-3 in thymocyte development. Immunity 2003, 19, 863-875.
10. Lim, K. C., Lakshmanan, G., Crawford, S. E., Gu, Y. et al., Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat. Genet. 2000, 25, 209-212.
11. Asselin-Labat, M. L., Mammary stem and progenitor cells: critical role of the transcription factor Gata-3. Med. Sci. (Paris) 2007, 23, 1077-1080.
12. Shackleton, M., Vaillant, F., Simpson, K. J., Stingl, J. et al., Generation of a functional mammary gland from a single stem cell. Nature 2006, 439, 84-88.
13. Lim, E., Wu, D., Pal, B., Bouras, T. et al., Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res. 2010, 12, R21.
14. Pavlou, M. P., Diamandis, E. P., The cancer cell secretome: A good source for discovering biomarkers? J. Proteomics 2010, 73, 1896-1906.
15. Alphonso, A., Alahari, S. K., Stromal cells and integrins: conforming to the needs of the tumor microenvironment. Neoplasia 2009, 11, 1264-1271.
16. Asselin-Labat, M. L., Shackleton, M., Stingl, J., Vaillant, F. et al., Steroid hormone receptor status of mouse mammary stem cells. J. Natl. Cancer Inst. 2006, 98, 1011-1014.
17. Foster, S. A., Galloway, D. A., Human papillomavirus type 16 E7 alleviates a proliferation block in early passage human mammary epithelial cells. Oncogene 1996, 12, 1773-1779.
18. Goode, R. J., Simpson, R. J., Purification of basolateral integral membrane proteins by cationic colloidal silica-based apical membrane subtraction. Methods Mol. Biol. 2009, 528, 177-187.
19. Simpson, R. J., Connolly, L. M., Eddes, J. S., Pereira, J. J. et al., Proteomic analysis of the human colon carcinoma cell line (LIM 1215): development of a membrane protein database. Electrophoresis 2000, 21, 1707-1732.
20. Eddes, J. S., Kapp, E. A., Frecklington, D. F., Connolly, L. M. et al., CHOMPER: a bioinformatic tool for rapid validation of tandem mass spectrometry search results associated with high-throughput proteomic strategies. Proteomics 2002, 2, 1097-1103.
21. Greening, D. W., Glenister, K. M., Kapp, E. A., Moritz, R. L. et al., Comparison of human platelet membrane-cytoskeletal proteins with the plasma proteome: towards understanding the platelet-plasma nexus. Proteomics Clin. Appl. 2008, 2, 63-77.
22. Kapp, E. A., Schutz, F., Connolly, L. M., Chakel, J. A. et al., An evaluation, comparison, and accurate benchmarking of several publicly available MS/MS search algorithms: sensitivity and specificity analysis. Proteomics 2005, 5, 3475-3490.
23. Mathias, R. A., Chen, Y. S., Wang, B., Ji, H. et al., Extracellular remodelling during oncogenic Ras-induced epithelial-mesenchymal transition facilitates MDCK cell migration. J. Proteome Res. 2010, 9, 1007-1019.
24. Old, W. M., Meyer-Arendt, K., Aveline-Wolf, L., Pierce, K. G. et al., Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol. Cell. Proteomics 2005, 4, 1487-1502.
25. Bachelard-Cascales, E., Chapellier, M., Delay, E., Pochon, G. et al., The CD10 enzyme is a key player to identify and regulate human mammary stem cells. Stem Cells 2010, 28, 1081-1088.
26. LaBarge, M. A., Nelson, C. M., Villadsen, R., Fridriksdottir, A. et al., Human mammary progenitor cell fate decisions are products of interactions with combinatorial microenvironments. Integr. Biol. 2009, 1, 70-79.
27. Emanuelsson, O., Brunak, S., von Heijne, G., Nielsen, H., Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007, 2, 953-971.
28. Nickel, W., The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur. J. Biochem. 2003, 270, 2109-2119.
29. Mathivanan, S., Ji, H., Simpson, R. J., Exosomes: extracellular organelles important in intercellular communication. J Proteomics 2010, 73, 1907-1920.
30. Simpson, R. J., Lim, J. W., Moritz, R. L., Mathivanan, S., Exosomes: proteomic insights and diagnostic potential. Exp. Rev. Proteomics 2009, 6, 267-283.
31. Chen, Y., Yu, P., Luo, J., Jiang, Y., Secreted protein prediction system combining CJ-SPHMM, TMHMM, and PSORT. Mamm. Genome 2003, 14, 859-865.
32. Carvalho, P. C., Hewel, J., Barbosa, V. C., Yates, J. R., 3rd, Identifying differences in protein expression levels by spectral counting and feature selection. Genet. Mol. Res. 2008, 7, 342-356.
33. Choi, H., Fermin, D., Nesvizhskii, A. I., Significance analysis of spectral count data in label-free shotgun proteomics. Mol. Cell. Proteomics 2008, 7, 2373-2385.
34. Zybailov, B., Coleman, M. K., Florens, L., Washburn, M. P., Correlation of relative abundance ratios derived from peptide ion chromatograms and spectrum counting for quantitative proteomic analysis using stable isotope labeling. Anal. Chem. 2005, 77, 6218-6224.
35. Nusse, R., Wnt signaling and stem cell control. Cell Res. 2008, 18, 523-527.
36. Genander, M., Frisen, J., Ephrins and Eph receptors in stem cells and cancer. Curr. Opin. Cell Biol. 2010, 22, 611-616.
37. Raymond, K., Deugnier, M. A., Faraldo, M. M., Glukhova, M. A., Adhesion within the stem cell niches. Curr. Opin. Cell Biol. 2009, 21, 623-629.
38. Kouros-Mehr, H., Werb, Z., Candidate regulators of mammary branching morphogenesis identified by genome-wide transcript analysis. Dev. Dyn. 2006, 235, 3404-3412.
39. Kendrick, H., Regan, J. L., Magnay, F. A., Grigoriadis, A. et al., Transcriptome analysis of mammary epithelial subpopulations identifies novel determinants of lineage commitment and cell fate. BMC Genomics 2008, 9, 591.
40. Pasquale, E. B., Eph-ephrin bidirectional signaling in physiology and disease. Cell 2008, 133, 38-52.
41. Nikolova, Z., Djonov, V., Zuercher, G., Andres, A. C., Ziemiecki, A., Cell-type specific and estrogen dependent expression of the receptor tyrosine kinase EphB4 and its ligand ephrin-B2 during mammary gland morphogenesis. J. Cell Sci. 1998, 111, 2741-2751.
42. Munarini, N., Jager, R., Abderhalden, S., Zuercher, G. et al., Altered mammary epithelial development, pattern formation and involution in transgenic mice expressing the EphB4 receptor tyrosine kinase. J. Cell Sci. 2002, 115, 25-37.
43. Himanen, J. P., Chumley, M. J., Lackmann, M., Li, C. et al., Repelling class discrimination: ephrin-A5 binds to and activates EphB2 receptor signaling. Nat. Neurosci. 2004, 7, 501-509.
44. Hynes, R. O., Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110, 673-687.
45. Fassler, R., Meyer, M., Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev. 1995, 9, 1896-1908.
46. Taddei, I., Deugnier, M. A., Faraldo, M. M., Petit, V. et al., Beta1 integrin deletion from the basal compartment of the mammary epithelium affects stem cells. Nat. Cell Biol. 2008, 10, 716-722.
47. Chen, C., Sheppard, D., Identification and molecular characterization of multiple phenotypes in integrin knockout mice. Methods Enzymol. 2007, 426, 291-305.
48. Bosman, F. T., Stamenkovic, I., Functional structure and composition of the extracellular matrix. J. Pathol. 2003, 200, 423-428.
49. Lu, X., Borchers, A. G., Jolicoeur, C., Rayburn, H. et al., PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 2004, 430, 93-98.
50. Mathivanan, S., Simpson, R. J., ExoCarta: a compendium of exosomal proteins and RNA. Proteomics 2009, 9, 4997-5000.
51. Kikuchi, A., Yamamoto, H., Sato, A., Selective activation mechanisms of Wnt signaling pathways. Trends Cell Biol. 2009, 19, 119-129.
52. van Amerongen, R., Nusse, R., Towards an integrated view of Wnt signaling in development. Development 2009, 136, 3205-3214.
53. Haegebarth, A., Clevers, H., Wnt signaling, lgr5, and stem cells in the intestine and skin. Am. J. Pathol. 2009, 174, 715-721.
54. He, S., Nakada, D., Morrison, S. J., Mechanisms of stem cell self-renewal. Annu. Rev. Cell Dev. Biol. 2009, 25, 377-406.
55. Reya, T., Clevers, H., Wnt signalling in stem cells and cancer. Nature 2005, 434, 843-850.
56. Narita, T., Sasaoka, S., Udagawa, K., Ohyama, T. et al., Wnt10a is involved in AER formation during chick limb development. Dev. Dyn. 2005, 233, 282-287.
57. Zeng, Y. A., Nusse, R., Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell 2010, 6, 568-577.
58. Buhler, T. A., Dale, T. C., Kieback, C., Humphreys, R. C., Rosen, J. M., Localization and quantification of Wnt-2 gene expression in mouse mammary development. Dev. Biol. 1993, 155, 87-96.
59. Gavin, B. J., McMahon, A. P., Differential regulation of the Wnt gene family during pregnancy and lactation suggests a role in postnatal development of the mammary gland. Mol. Cell. Biol. 1992, 12, 2418-2423.
60. Huguet, E. L., McMahon, J. A., McMahon, A. P., Bicknell, R., Harris, A. L., Differential expression of human Wnt genes 2, 3, 4, and 7B in human breast cell lines and normal and disease states of human breast tissue. Cancer Res. 1994, 54, 2615-2621.
61. Lane, T. F., Leder, P., Wnt-10b directs hypermorphic development and transformation in mammary glands of male and female mice. Oncogene 1997, 15, 2133-2144.
62. Olson, D. J., Papkoff, J., Regulated expression of Wnt family members during proliferation of C57mg mammary cells. Cell Growth Differ. 1994, 5, 197-206.
63. Weber-Hall, S. J., Phippard, D. J., Niemeyer, C. C., Dale, T. C., Developmental and hormonal regulation of Wnt gene expression in the mouse mammary gland. Differentiation 1994, 57, 205-214.
64. Flaherty, M. P., Dawn, B., Noncanonical Wnt11 signaling and cardiomyogenic differentiation. Trends Cardiovasc. Med. 2008, 18, 260-268.
65. Gros, J., Serralbo, O., Marcelle, C., WNT11 acts as a directional cue to organize the elongation of early muscle fibres. Nature 2009, 457, 589-593.
66. Tao, Q., Yokota, C., Puck, H., Kofron, M. et al., Maternal wnt11 activates the canonical Wnt signaling pathway required for axis formation in Xenopus embryos. Cell 2005, 120, 857-871.
67. Bovolenta, P., Esteve, P., Ruiz, J. M., Cisneros, E., Lopez-Rios, J., Beyond Wnt inhibition: new functions of secreted Frizzled-related proteins in development and disease. J. Cell Sci. 2008, 121, 737-746.
68. Kawano, Y., Kypta, R., Secreted antagonists of the Wnt signalling pathway. J. Cell Sci. 2003, 116, 2627-2634.
69. Byun, T., Karimi, M., Marsh, J. L., Milovanovic, T. et al., Expression of secreted Wnt antagonists in gastrointestinal tissues: potential role in stem cell homeostasis. J. Clin. Pathol. 2005, 58, 515-519.
70. Chen, Y. S., Mathias, R. A., Mathivanan, S., Kapp, E. A. et al., Proteomics profiling of Madin-Darby canine kidney plasma membranes reveals Wnt-5a involvement during oncogenic H-Ras/TGF-beta-mediated epithelial-mesenchymal transition. Mol. Cell. Proteomics 2011, 10, M110 001131.