Contribution of phosphoproteomics in understanding SRC signaling in normal and tumor cells

Proteomics

Volumn 15, Issue 2-3, 2015, Pages 232-244

  Sirvent, Audrey ^a   Urbach, Serge ^b   Roche, Serge ^a  

^a Centre National de la Recherche Scientifique   (France)

^b CNRS   (France)

Author keywords

Cancer; Cell biology; Cell signaling; Phosphoproteomics; SRC; Tyrosine kinase

Indexed keywords

CELL SURFACE RECEPTOR; GROWTH FACTOR; PROTEIN TYROSINE KINASE;

CARCINOGENESIS; CELL METABOLISM; CELL TRANSFORMATION; COMPREHENSION; CONTROLLED STUDY; CYTOLOGY; DNA SYNTHESIS; EUKARYOTIC CELL; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; NON-TRANSFORMED CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; TRANSFORMED CELL; ANIMAL; ENZYMOLOGY; METABOLISM; NEOPLASM; PHOSPHORYLATION; PROCEDURES;

ANIMALS; CARCINOGENESIS; HUMANS; NEOPLASMS; PHOSPHORYLATION; PROTEOMICS; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84921293145     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400162     Document Type: Review

References (106)

1. Thomas, S. M., Brugge, J. S., Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 1997, 13, 513-609.
2. Yeatman, T. J., A renaissance for SRC. Nat. Rev. Cancer 2004, 4, 470-480.
3. Xu, W., Harrison, S. C., Eck, M. J., Three-dimensional structure of the tyrosine kinase c-Src. Nature 1997, 385, 595-602.
4. Sicheri, F., Moarefi, I., Kuriyan, J., Crystal structure of the Src family tyrosine kinase Hck. Nature 1997, 385, 602-609.
5. Boggon, T. J., Eck, M. J., Structure and regulation of Src family kinases. Oncogene 2004, 23, 7918-7927.
6. Nada, S., Okada, M., MacAuley, A., Cooper, J. A., Nakagawa, H., Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature 1991, 351, 69-72.
7. Perez, Y., Maffei, M., Igea, A., Amata, I. et al., Lipid binding by the unique and SH3 domains of c-Src suggests a new regulatory mechanism. Sci. Rep. 2013, 3, 1295.
8. Imamoto, A., Soriano, P., Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell 1993, 73, 1117-1124.
9. Nada, S., Yagi, T., Takeda, H., Tokunaga, T. et al., Constitutive activation of Src family kinases in mouse embryos that lack Csk. Cell 1993, 73, 1125-1135.
10. Stewart, R. A., Li, D. M., Huang, H., Xu, T., A genetic screen for modifiers of the lats tumor suppressor gene identifies C-terminal Src kinase as a regulator of cell proliferation in Drosophila. Oncogene 2003, 22, 6436-6444.
11. Read, R. D., Bach, E. A., Cagan, R. L., Drosophila C-terminal Src kinase negatively regulates organ growth and cell proliferation through inhibition of the Src, Jun N-terminal kinase, and STAT pathways. Mol. Cell. Biol. 2004, 24, 6676-6689.
12. Soriano, P., Montgomery, C., Geske, R., Bradley, A., Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 1991, 64, 693-702.
13. Klinghoffer, R. A., Sachsenmaier, C., Cooper, J. A., Soriano, P., Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J. 1999, 18, 2459-2471.
14. Twamley-Stein, G. M., Pepperkok, R., Ansorge, W., Courtneidge, S. A., The Src family tyrosine kinases are required for platelet-derived growth factor-mediated signal transduction in NIH 3T3 cells. Proc. Natl. Acad. Sci. USA 1993, 90, 7696-7700.
15. Roche, S., Koegl, M., Barone, M. V., Roussel, M. F., Courtneidge, S. A., DNA synthesis induced by some but not all growth factors requires Src family protein tyrosine kinases. Mol. Cell. Biol. 1995, 15, 1102-1109.
16. Broome, M. A., Hunter, T., Requirement for c-Src catalytic activity and the SH3 domain in platelet- derived growth factor BB and epidermal growth factor mitogenic signaling. J. Biol. Chem. 1996, 271, 16798-16806.
17. Sieg, D. J., Hauck, C. R., Ilic, D., Klingbeil, C. K. et al., FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell. Biol. 2000, 2, 249-256.
18. Veracini, L., Franco, M., Boureux, A., Simon, V. et al., Two distinct pools of Src family tyrosine kinases regulate PDGF-induced DNA synthesis and actin dorsal ruffles. J. Cell. Sci. 2006, 20, 2921-2934.
19. Roche, S., Fumagalli, S., Courtneidge, S. A., Requirement for Src family protein tyrosine kinases in G2 for fibroblast cell division. Science 1995, 269, 1567-1569.
20. Tominaga, T., Sahai, E., Chardin, P., McCormick, F. et al., Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol. Cell 2000, 5, 13-25.
21. Kasahara, K., Nakayama, Y., Nakazato, Y., Ikeda, K. et al., Src signaling regulates completion of abscission in cytokinesis through ERK/MAPK activation at the midbody. J. Biol. Chem. 2007, 282, 5327-5339.
22. Summy, J. M., Gallick, G. E., Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev. 2003, 22, 337-358.
23. Han, N. M., Curley, S. A., Gallick, G. E., Differential activation of pp60(c-src) and pp62(c-yes) in human colorectal carcinoma liver metastases. Clin. Cancer Res. 1996, 2, 1397-1404.
24. Aligayer, H., Boyd, D. D., Heiss, M. M., Abdalla, E. K. et al., Activation of Src kinase in primary colorectal carcinoma: an indicator of poor clinical prognosis. Cancer 2002, 94, 344-351.
25. Zhang, X. H., Wang, Q., Gerald, W., Hudis, C. A. et al., Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell 2009, 16, 67-78.
26. Sirvent, A., Benistant, C., Roche, S., Oncogenic signaling by tyrosine kinases of the SRC family in advanced colorectal cancer. Am. J. Cancer Res. 2012, 2, 357-371.
27. Zhang, B., Wang, J., Wang, X., Zhu, J. et al., Proteogenomic characterization of human colon and rectal cancer. Nature 2014, 513, 382-387.
28. Sirvent, A., Benistant, C., Pannequin, J., Veracini, L. et al., Src family tyrosine kinases-driven colon cancer cell invasion is induced by Csk membrane delocalization. Oncogene 2010, 29, 1303-1315.
29. Cordero, J. B., Ridgway, R. A., Valeri, N., Nixon, C. et al., c-Src drives intestinal regeneration and transformation. EMBO J. 2014, 33, 1474-1491.
30. Kohlmaier, A., Fassnacht, C., Jin, Y., Reuter, H. et al., Src kinase function controls progenitor cell pools during regeneration and tumor onset in the Drosophila intestine. Oncogene 2014, doi: 10.1038/onc.2014.163.
31. Kopetz, S., Shah, A. N., Gallick, G. E., Src continues aging: current and future clinical directions. Clin. Cancer Res. 2007, 13, 7232-7236.
32. Abrahamsen, H., Vang, T., Tasken, K., Protein kinase A intersects SRC signaling in membrane microdomains. J. Biol. Chem. 2003, 278, 17170-17177.
33. Veracini, L., Franco, M., Boureux, A., Simon, V. et al., Two functionally distinct pools of Src kinases for PDGF receptor signalling. Biochem. Soc. Trans. 2005, 33, 1313-1315.
34. Mori, S., Ronnstrand, L., Yokote, K., Engstrom, A. et al., Identification of two juxtamembrane autophosphorylation sites in the PDGF beta-receptor; involvement in the interaction with Src family tyrosine kinases. EMBO J. 1993, 12, 2257-2264.
35. Olivera, A., Edsall, L., Poulton, S., Kazlauskas, A., Spiegel, S., Platelet-derived growth factor-induced activation of sphingosine kinase requires phosphorylation of the PDGF receptor tyrosine residue responsible for binding of PLCgamma. FASEB J. 1999, 13, 1593-1600
36. Rosenfeldt, H. M., Hobson, J. P., Maceyka, M., Olivera, A. et al., EDG-1 links the PDGF receptor to Src and focal adhesion kinase activation leading to lamellipodia formation and cell migration. FASE J. 2001, 15, 2649-2659
37. Shah, K., Vincent, F., Divergent roles of c-Src in controlling platelet-derived growth factor-dependent signaling in fibroblasts. Mol. Biol. Cell 2005, 16, 5418-5432.
38. Barone, M. V., Courtneidge, S. A., Myc but not Fos rescue of PDGF signalling block caused by kinase-inactive Src [see comments]. Nature 1995, 378, 509-512.
39. Blake, R. A., Broome, M. A., Liu, X., Wu, J. et al., SU6656, a selective src family kinase inhibitor, used to probe growth factor signaling. Mol. Cell. Biol. 2000, 20, 9018-9027.
40. Furstoss, O., Dorey, K., Simon, V., Barilla, D. et al., c-Abl is an effector of Src for growth factor-induced c-myc expression and DNA synthesis. EMBO J. 2002, 27, 514-524.
41. Boureux, A., Furstoss, O., Simon, V., Roche, S., c-Abl tyrosine kinase regulates a Rac/JNK and a Rac/Nox pathway for DNA synthesis and c-myc expression induced by growth factors. J. Cell Sci. 2005, 118, 3717-3726.
42. Broome, M. A., Courtneidge, S. A., No requirement for src family kinases for PDGF signaling in fibroblasts expressing SV40 large T antigen. Oncogene 2000, 19, 2867-2869.
43. Furstoss, O., Manes, G., Roche, S., Cyclin E and cyclin A are likely targets of Src for PDGF-induced DNA synthesis in fibroblasts. FEBS Lett. 2002, 526, 82-86.
44. Niu, G., Wright, K. L., Ma, Y., Wright, G. M. et al., Role of Stat3 in regulating p53 expression and function. Mol. Cell. Biol. 2005, 25, 7432-7440.
45. Quintavalle, M., Elia, L., Condorelli, G., Courtneidge, S. A., MicroRNA control of podosome formation in vascular smooth muscle cells in vivo and in vitro. J. Cell. Biol. 2010, 189, 13-22.
46. Reynolds, A. B., Kanner, S. B., Bouton, A. H., Schaller, M. D. et al., SRChing for the substrates of Src. Oncogene 2014, 33, 4537-4547.
47. Pelicci, G., Lanfrancone, L., Grignani, F., McGlade, J. et al., A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 1992, 70, 93-104.
48. Bowman, T., Broome, M. A., Sinibaldi, D., Wharton, W. et al., Stat3-mediated Myc expression is required for Src transformation and PDGF-induced mitogenesis. Proc. Natl. Acad. Sci. USA 2001, 98, 7319-7324.
49. Chiariello, M., Marinissen, M. J., Gutkind, J. S., Regulation of c-myc expression by PDGF through Rho GTPases. Nat. Cell. Biol. 2001, 3, 580-586.
50. Plattner, R., Kadlec, L., DeMali, K. A., Kazlauskas, A., Pendergast, A. M., c-Abl is activated by growth factors and Src family kinases and has a role in the cellular response to PDGF. Genes Dev. 1999, 13, 2400-2411.
51. Lock, P., Abram, C. L., Gibson, T., Courtneidge, S. A., A new method for isolating tyrosine kinase substrates used to identify fish, an SH3 and PX domain-containing protein, and Src substrate. EMBO J. 1998, 17, 4346-4357.
52. Courtneidge, S. A., Isolation of novel Src substrates. Biochem. Soc. Trans. 2003, 31, 25-28.
53. Seals, D. F., Azucena, E. F., Jr., Pass, I., Tesfay, L. et al., The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells. Cancer Cell 2005, 7, 155-165.
54. Franco, M., Furstoss, O., Simon, V., Benistant, C. et al., The adaptor protien Tom1L1 is a negative regulator of Src mitogenic signaling induced by growth factors. Mol. Biol. Cell 2006, 26, 1932-1947.
55. Collin, G., Franco, M., Simon, V., Benistant, C., Roche, S., The Tom1L1-clathrin heavy chain complex regulates membrane partitioning of the tyrosine kinase Src required for mitogenic and transforming activities. Mol. Cell. Biol. 2007, 27, 7631-7640.
56. Abram, C. L., Courtneidge, S. A., Src family tyrosine kinases and growth factor signaling. Exp. Cell Res. 2000, 254, 1-13.
57. Stephens, L. R., Anderson, K. E., Hawkins, P. T., Src family kinases mediate receptor-stimulated, phosphoinositide 3-kinase-dependent, tyrosine phosphorylation of dual adaptor for phosphotyrosine and 3-phosphoinositides-1 in endothelial and B cell lines. J. Biol. Chem. 2001, 276, 42767-42773.
58. Rebholz, H., Panasyuk, G., Fenton, T., Nemazanyy, I. et al., Receptor association and tyrosine phosphorylation of S6 kinases. FEBS J. 2006, 273, 2023-2036.
59. Kajita, M., Ikeda, W., Tamaru, Y., Takai, Y., Regulation of platelet-derived growth factor-induced Ras signaling by poliovirus receptor Necl-5 and negative growth regulator Sprouty2. Genes Cells 2007, 12, 345-357.
60. Nakata, S., Fujita, N., Kitagawa, Y., Okamoto, R. et al., Regulation of platelet-derived growth factor receptor activation by afadin through SHP-2: implications for cellular morphology. J. Biol. Chem. 2007, 282, 37815-37825.
61. Wang, Y., Zhou, K., Zeng, X., Lin, J., Zhan, X., Tyrosine phosphorylation of missing in metastasis protein is implicated in platelet-derived growth factor-mediated cell shape changes. J. Biol. Chem. 2007, 282, 7624-7631.
62. Daviau, A., Di Fruscio, M., Blouin, R., The mixed-lineage kinase DLK undergoes Src-dependent tyrosine phosphorylation and activation in cells exposed to vanadate or platelet-derived growth factor (PDGF). Cell. Signal. 2009, 21, 577-587.
63. Yu, J. A., Deakin, N. O., Turner, C. E., Paxillin-kinase-linker tyrosine phosphorylation regulates directional cell migration. Mol. Biol. Cell 2009, 20, 4706-4719.
64. Engholm-Keller, K., Larsen, M. R., Technologies and challenges in large-scale phosphoproteomics. Proteomics 2013, 13, 910-931.
65. Villen, J., Beausoleil, S. A., Gerber, S. A., Gygi, S. P., Large-scale phosphorylation analysis of mouse liver. Proc. Natl. Acad. Sci. USA 2007, 104, 1488-1493.
66. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C. et al., Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 2010, 3, ra3.
67. Rush, J., Moritz, A., Lee, K. A., Guo, A. et al., Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 2005, 23, 94-101.
68. Blagoev, B., Ong, S. E., Kratchmarova, I., Mann, M., Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat. Biotechnol. 2004, 22, 1139-1145.
69. Zhang, G., Neubert, T. A., Comparison of three quantitative phosphoproteomic strategies to study receptor tyrosine kinase signaling. J. Proteome Res. 2011, 10, 5454-5462.
70. Amanchy, R., Zhong, J., Hong, R., Kim, J. H. et al., Identification of c-Src tyrosine kinase substrates in platelet-derived growth factor receptor signaling. Mol. Oncol. 2009, 3, 439-450.
71. Knowlton, M. L., Selfors, L. M., Wrobel, C. N., Gu, T. L. et al., Profiling Y561-dependent and -independent substrates of CSF-1R in epithelial cells. PLoS One 2010, 5, e13587.
72. Courtneidge, S. A., Dhand, R., Pilat, D., Twamley, G. M. et al., Activation of Src family kinases by colony stimulating factor-1, and their association with its receptor. EMBO J. 1993, 12, 943-950.
73. Luo, W., Slebos, R. J., Hill, S., Li, M. et al., Global impact of oncogenic Src on a phosphotyrosine proteome. J. Proteome Res. 2008, 7, 3447-3460.
74. Amanchy, R., Zhong, J., Molina, H., Chaerkady, R. et al., Identification of c-Src tyrosine kinase substrates using mass spectrometry and peptide microarrays. J. Proteome Res. 2008, 7, 3900-3910.
75. Qiao, Y., Molina, H., Pandey, A., Zhang, J., Cole, P. A., Chemical rescue of a mutant enzyme in living cells. Science 2006, 311, 1293-1297.
76. Ferrando, I. M., Chaerkady, R., Zhong, J., Molina, H. et al., Identification of targets of c-Src tyrosine kinase by chemical complementation and phosphoproteomics. Mol. Cell. Proteomics 2012, 11, 355-369.
77. Kim, L. C., Song, L., Haura, E. B., Src kinases as therapeutic targets for cancer. Nat. Rev. Clin. Oncol. 2009, 6, 587-595.
78. Naudin, C., Sirvent, A., Leroy, C., Larive, R. et al., SLAP displays tumour suppressor functions in colorectal cancer via destabilization of the SRC substrate EPHA2. Nat. Commun. 2014, 5, doi: 10.1038/ncomms4159.
79. Leroy, C., Fialin, C., Sirvent, A., Simon, V. et al., Quantitative phosphoproteomics reveals a cluster of tyrosine kinases that mediates SRC invasive activity in advanced colon carcinoma cells. Cancer Res. 2009, 69, 2279-2286.
80. Kruger, M., Moser, M., Ussar, S., Thievessen, I. et al., SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function. Cell 2008, 134, 353-364.
81. Sirvent, A., Vigy, O., Orsetti, B., Urbach, S., Roche, S., Analysis of SRC oncogenic signaling in colorectal cancer by Stable Isotope Labeling with heavy Amino acids in mouse Xenografts. Mol. Cell. Proteomics 2012, 11, 1937-1950.
82. Frame, M. C., Newest findings on the oldest oncogene; how activated src does it. J. Cell Sci. 2004, 117, 989-998.
83. Qian, X., Li, G., Vass, W. C., Papageorge, A. et al., The Tensin-3 protein, including its SH2 domain, is phosphorylated by Src and contributes to tumorigenesis and metastasis. Cancer Cell 2009, 16, 246-258.
84. Kelber, J. A., Reno, T., Kaushal, S., Metildi, C. et al., KRas induces a Src/PEAK1/ErbB2 kinase amplification loop that drives metastatic growth and therapy resistance in pancreatic cancer. Cancer Res. 2012, 72, 2554-2564.
85. Croucher, D. R., Hochgrafe, F., Zhang, L., Liu, L. et al., Involvement of Lyn and the atypical kinase SgK269/PEAK1 in a basal breast cancer signaling pathway. Cancer Res. 2013, 73, 1969-1980.
86. Joffre, C., Barrow, R., Menard, L., Calleja, V. et al., A direct role for Met endocytosis in tumorigenesis. Nat. Cell Biol. 2011, 13, 827-837.
87. Hochgrafe, F., Zhang, L., O'Toole, S. A., Browne, B. C. et al., Tyrosine phosphorylation profiling reveals the signaling network characteristics of Basal breast cancer cells. Cancer Res. 2010, 70, 9391-9401.
88. Sancier, F., Dumont, A., Sirvent, A., Paquay de Plater, L. et al., Specific oncogenic activity of the Src-family tyrosine kinase c-Yes in colon carcinoma cells. PLoS One 2011, 6, e17237.
89. Vermeulen, L., de Sousa, E. M. F., van der Heijden, M., Cameron, K. et al., Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 2010, 12, 468-476.
90. Straussman, R., Morikawa, T., Shee, K., Barzily-Rokni, M. et al., Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012, 487, 500-504.
91. Rikova, K., Guo, A., Zeng, Q., Possemato, A. et al., Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007, 131, 1190-1203.
92. Wu, Z., Doondeea, J. B., Gholami, A. M., Janning, M. C. et al., Quantitative chemical proteomics reveals new potential drug targets in head and neck cancer. Mol. Cell. Proteomics 2011, 10, M111 011635.
93. Menges, C. W., Chen, Y., Mossman, B. T., Chernoff, J. et al., A phosphotyrosine proteomic screen identifies multiple tyrosine kinase signaling pathways aberrantly activated in malignant mesothelioma. Genes Cancer 2010, 1, 493-505.
94. Drake, J. M., Graham, N. A., Stoyanova, T., Sedghi, A. et al., Oncogene-specific activation of tyrosine kinase networks during prostate cancer progression. Proc. Natl. Acad. Sci. USA 2012, 109, 1643-1648.
95. Drake, J. M., Graham, N. A., Lee, J. K., Stoyanova, T. et al., Metastatic castration-resistant prostate cancer reveals intrapatient similarity and interpatient heterogeneity of therapeutic kinase targets. Proc. Natl. Acad. Sci. USA 2013, 110, E4762-4769.
96. Rubbi, L., Titz, B., Brown, L., Galvan, E. et al., Global phosphoproteomics reveals crosstalk between Bcr-Abl and negative feedback mechanisms controlling Src signaling. Sci. Signal. 2011, 4, ra18.
97. Suwaki, N., Vanhecke, E., Atkins, K. M., Graf, M. et al., A HIF-regulated VHL-PTP1B-Src signaling axis identifies a therapeutic target in renal cell carcinoma. Sci. Transl. Med. 2011, 3, 85ra47.
98. Zanivan, S., Meves, A., Behrendt, K., Schoof, E. M. et al., In vivo SILAC-based proteomics reveals phosphoproteome changes during mouse skin carcinogenesis. Cell Rep. 2013, 3, 552-566.
99. Armaiz-Pena, G. N., Allen, J. K., Cruz, A., Stone, R. L. et al., Src activation by beta-adrenoreceptors is a key switch for tumour metastasis. Nat. Commun. 2013, 4, 1403.
100. Beristain, A. G., Molyneux, S. D., Joshi, P. A., Pomroy, N. C. et al., PKA signaling drives mammary tumorigenesis through Src. Oncogene 2014 (in press), doi: 10.1038/onc.2014.41 [Epub ahead of print].
101. Rexer, B. N., Ham, A. J., Rinehart, C., Hill, S. et al., Phosphoproteomic mass spectrometry profiling links Src family kinases to escape from HER2 tyrosine kinase inhibition. Oncogene, 30, 4163-4174.
102. Zhang, S., Huang, W. C., Li, P., Guo, H. et al., Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways. Nat. Med. 2011, 17, 461-469.
103. Mahon, F. X., Hayette, S., Lagarde, V., Belloc, F. et al., Evidence that resistance to nilotinib may be due to BCR-ABL, Pgp, or Src kinase overexpression. Cancer Res. 2008, 68, 9809-9816.
104. Gioia, R., Leroy, C., Drullion, C., Lagarde, V. et al., Quantitative phosphoproteomics revealed interplay between Syk and Lyn in the resistance to nilotinib in chronic myeloid leukemia cells. Blood 2011, 118, 2211-2221.
105. Geiger, T., Cox, J., Ostasiewicz, P., Wisniewski, J. R., Mann, M., Super-SILAC mix for quantitative proteomics of human tumor tissue. Nat. Methods 2010, 7, 383-385.
106. Monetti, M., Nagaraj, N., Sharma, K., Mann, M., Large-scale phosphosite quantification in tissues by a spike-in SILAC method. Nat. Methods 2011, 8, 655-658.