Comprehensive quantitative comparison of the membrane proteome, phosphoproteome, and sialiome of human embryonic and neural stem cells

Molecular and Cellular Proteomics

Volumn 13, Issue 1, 2014, Pages 311-328

  Melo Braga, Marcella Nunes ^a   Schulz, Melanie ^a   Liu, Qiuyue ^b   Swistowski, Andrzej ^b   Palmisano, Giuseppe ^a,c   Engholm Keller, Kasper ^a,d   Jakobsen, Lene ^a   Zeng, Xianmin ^b   Larsen, Martin Røssel ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d CHILDREN'S MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CELL MEMBRANE PROTEIN; CELL SURFACE MARKER; CRUMBS 2; GLYCOPEPTIDE; PEPTIDE; PHOSPHOPEPTIDE; PHOSPHOPROTEOME; PROTEOME; SIALIOME; SIALOGLYCOPROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOCYTOCHEMISTRY; INTRACELLULAR SIGNALING; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEOMICS; QUANTITATIVE STUDY; SIALYLATION; UPREGULATION;

CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; GLYCOPEPTIDES; HUMANS; MEMBRANE PROTEINS; NEURAL STEM CELLS; NEURONS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; SIGNAL TRANSDUCTION;

EID: 84891777324     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.026898     Document Type: Article

References (100)

1. Gage, F. H. (2000) Mammalian neural stem cells. Science 287, 1433-1438
2. Carpenter, M. K., Rosler, E., and Rao, M. S. (2003) Characterization and differentiation of human embryonic stem cells. Cloning Stem Cells 5, 79-88
3. Nagano, K., Yoshida, Y., and Isobe, T. (2008) Cell surface biomarkers of embryonic stem cells. Proteomics 8, 4025-4035
4. Shmelkov, S. V., Butler, J. M., Hooper, A. T., Hormigo, A., Kushner, J., Milde, T., St Clair, R., Baljevic, M., White, I., Jin, D. K., Chadburn, A., Murphy, A. J., Valenzuela, D. M., Gale, N. W., Thurston, G., Yancopoulos, G. D., D'Angelica, M., Kemeny, N., Lyden, D., and Rafii, S. (2008) CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J. Clin. Invest. 118, 2111-2120
5. Hunter, T. (2000) Signaling-2000 and beyond. Cell 100, 113-127
6. Ohtsubo, K., and Marth, J. D. (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126, 855-867
7. Rudd, P. M., Elliott, T., Cresswell, P., Wilson, I. A., and Dwek, R. A. (2001) Glycosylation and the immune system. Science 291, 2370-2376
8. Helenius, A., and Aebi, M. (2001) Intracellular functions of N-linked glycans. Science 291, 2364-2369
9. Blix, G., Lindberg, E., Odin, L., and Werner, I. (1955) Sialic acids. Nature 175, 340-341
10. Cunningham, B. A., Hemperly, J. J., Murray, B. A., Prediger, E. A., Brackenbury, R., and Edelman, G. M. (1987) Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236, 799-806
11. Schauer, R. (2000) Achievements and challenges of sialic acid research. Glycoconj. J. 17, 485-499
12. Varki, N. M., and Varki, A. (2007) Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab. Invest. 87, 851-857
13. Muhlenhoff, M., Oltmann-Norden, I., Weinhold, B., Hildebrandt, H., and Gerardy-Schahn, R. (2009) Brain development needs sugar: the role of polysialic acid in controlling NCAM functions. Biol. Chem. 390, 567-574
14. Gasic, G., and Gasic, T. (1962) Removal of sialic acid from the cell coat in tumor cells and vascular endothelium, and its effects on metastasis. Proc. Natl. Acad. Sci. U.S.A. 48, 1172-1177
15. Brill, L. M., Xiong, W., Lee, K. B., Ficarro, S. B., Crain, A., Xu, Y., Terskikh, A., Snyder, E. Y., and Ding, S. (2009) Phosphoproteomic analysis of human embryonic stem cells. Cell Stem Cell 5, 204-213
16. Fathi, A., Pakzad, M., Taei, A., Brink, T. C., Pirhaji, L., Ruiz, G., Sharif Tabe Bordbar, M., Gourabi, H., Adjaye, J., Baharvand, H., and Salekdeh, G. H. (2009) Comparative proteome and transcriptome analyses of embryonic stem cells during embryoid body-based differentiation. Proteomics 9, 4859-4870
17. Rigbolt, K. T., Prokhorova, T. A., Akimov, V., Henningsen, J., Johansen, P. T., Kratchmarova, I., Kassem, M., Mann, M., Olsen, J. V., and Blagoev, B. (2011) System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci. Signal. 4, rs3
18. Schulz, T. C., Swistowska, A. M., Liu, Y., Swistowski, A., Palmarini, G., Brimble, S. N., Sherrer, E., Robins, A. J., Rao, M. S., and Zeng, X. (2007) A large-scale proteomic analysis of human embryonic stem cells. BMC Genomics 8, 478
19. Swaney, D. L., Wenger, C. D., Thomson, J. A., and Coon, J. J. (2009) Human embryonic stem cell phosphoproteome revealed by electron transfer dissociation tandem mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 106, 995-1000
20. Van Hoof, D., Munoz, J., Braam, S. R., Pinkse, M. W., Linding, R., Heck, A. J., Mummery, C. L., and Krijgsveld, J. (2009) Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 5, 214-226
21. Chaerkady, R., Kerr, C. L., Marimuthu, A., Kelkar, D. S., Kashyap, M. K., Gucek, M., Gearhart, J. D., and Pandey, A. (2009) Temporal analysis of neural differentiation using quantitative proteomics. J. Proteome Res. 8, 1315-1326
22. Chaerkady, R., Letzen, B., Renuse, S., Sahasrabuddhe, N. A., Kumar, P., All, A. H., Thakor, N. V., Delanghe, B., Gearhart, J. D., Pandey, A., and Kerr, C. L. (2011) Quantitative temporal proteomic analysis of human embryonic stem cell differentiation into oligodendrocyte progenitor cells. Proteomics 11, 4007-4020
23. Giancotti, F. G., and Ruoslahti, E. (1999) Integrin signaling. Science 285, 1028-1032
24. Swistowski, A., Peng, J., Han, Y., Swistowska, A. M., Rao, M. S., and Zeng, X. (2009) Xeno-free defined conditions for culture of human embryonic stem cells, neural stem cells and dopaminergic neurons derived from them. PLoS One 4, e6233
25. Zeng, X., Miura, T., Luo, Y., Bhattacharya, B., Condie, B., Chen, J., Ginis, I., Lyons, I., Mejido, J., Puri, R. K., Rao, M. S., and Freed, W. J. (2004) Properties of pluripotent human embryonic stem cells BG01 and BG02. Stem Cells 22, 292-312
26. Swistowska, A. M., da Cruz, A. B., Han, Y., Swistowski, A., Liu, Y., Shin, S., Zhan, M., Rao, M. S., and Zeng, X. (2010) Stage-specific role for shh in dopaminergic differentiation of human embryonic stem cells induced by stromal cells. Stem Cells Dev. 19, 71-82
27. Swistowski, A., Peng, J., Liu, Q., Mali, P., Rao, M. S., Cheng, L., and Zeng, X. (2010) Efficient generation of functional dopaminergic neurons from human induced pluripotent stem cells under defined conditions. Stem Cells 28, 1893-1904
28. Fujiki, Y., Hubbard, A. L., Fowler, S., and Lazarow, P. B. (1982) Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93, 97-102
29. Hsu, J. L., Huang, S. Y., Chow, N. H., and Chen, S. H. (2003) Stableisotope dimethyl labeling for quantitative proteomics. Anal. Chem. 75, 6843-6852
30. Boersema, P. J., Raijmakers, R., Lemeer, S., Mohammed, S., and Heck, A. J. (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat. Protoc. 4, 484-494
31. Thingholm, T. E., Jensen, O. N., Robinson, P. J., and Larsen, M. R. (2008) SIMAC (sequential elution from IMAC), a phosphoproteomics strategy for the rapid separation of monophosphorylated from multiply phosphorylated peptides. Mol. Cell. Proteomics 7, 661-671
32. Engholm-Keller, K., Hansen, T. A., Palmisano, G., and Larsen, M. R. (2011) Multidimensional strategy for sensitive phosphoproteomics incorporating protein prefractionation combined with SIMAC, HILIC, and TiO(2) chromatography applied to proximal EGF signaling. J. Proteome Res. 10, 5383-5397
33. Larsen, M. R., Jensen, S. S., Jakobsen, L. A., and Heegaard, N. H. (2007) Exploring the sialiome using titanium dioxide chromatography and mass spectrometry. Mol. Cell. Proteomics 6, 1778-1787
34. Larsen, M. R., Thingholm, T. E., Jensen, O. N., Roepstorff, P., and Jorgensen, T. J. (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 4, 873-886
35. Palmisano, G., Parker, B. L., Engholm-Keller, K., Lendal, S. E., Kulej, K., Schulz, M., Schwammle, V., Graham, M. E., Saxtorph, H., Cordwell, S. J., and Larsen, M. R. (2012) A novel method for the simultaneous enrichment, identification and quantification of phosphopeptides and sialylated glycopeptides applied to a temporal profile of mouse brain development. Mol. Cell. Proteomics 11, 1191-202
36. McNulty, D. E., and Annan, R. S. (2008) Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection. Mol. Cell. Proteomics 7, 971-980
37. Spivak, M., Weston, J., Bottou, L., Kall, L., and Noble, W. S. (2009) Improvements to the percolator algorithm for Peptide identification from shotgun proteomics data sets. J. Proteome Res. 8, 3737-3745
38. Blagoev, B., Ong, S. E., Kratchmarova, I., and Mann, M. (2004) Temporal analysis of phosphotyrosine-dependent signaling networks by quantitative proteomics. Nat. Biotechnol. 22, 1139-1145
39. Savitski, M. M., Lemeer, S., Boesche, M., Lang, M., Mathieson, T., Bantscheff, M., and Kuster, B. (2011) Confident phosphorylation site localization using the Mascot Delta Score. Mol. Cell Proteomics 10, M110 003830
40. Taus, T., Kocher, T., Pichler, P., Paschke, C., Schmidt, A., Henrich, C., and Mechtler, K. (2011) Universal and confident phosphorylation site localization using phosphoRS. J. Proteome Res 10, 5354-5362
41. Schwartz, D., and Gygi, S. P. (2005) An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat. Biotechnol. 23, 1391-1398
42. Aye, T. T., Low, T. Y., Bjorlykke, Y., Barsnes, H., Heck, A. J., and Berven, F. S. (2012) Use of stable isotope dimethyl labeling coupled to selected reaction monitoring to enhance throughput by multiplexing relative quantitation of targeted proteins. Anal. Chem. 84, 4999-5006
43. MacLean, B., Tomazela, D. M., Shulman, N., Chambers, M., Finney, G. L., Frewen, B., Kern, R., Tabb, D. L., Liebler, D. C., and MacCoss, M. J. (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966-968
44. Thingholm, T. E., Larsen, M. R., Ingrell, C. R., Kassem, M., and Jensen, O. N. (2008) TiO(2)-based phosphoproteomic analysis of the plasma membrane and the effects of phosphatase inhibitor treatment. J. Proteome Res. 7, 3304-3313
45. Palmisano, G., Lendal, S. E., Engholm-Keller, K., Leth-Larsen, R., Parker, B. L., and Larsen, M. R. (2010) Selective enrichment of sialic acidcontaining glycopeptides using titanium dioxide chromatography with analysis by HILIC and mass spectrometry. Nat. Protoc. 5, 1974-1982
46. Palmisano, G., Lendal, S. E., and Larsen, M. R. (2011) Titanium dioxide enrichment of sialic acid-containing glycopeptides. Methods Mol. Biol. 753, 309-322
47. Casey, P. J. (1995) Protein lipidation in cell signaling. Science 268, 221-225
48. Kupzig, S., Korolchuk, V., Rollason, R., Sugden, A., Wilde, A., and Banting, G. (2003) Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 4, 694-709
49. Ratnoff, W. D., Knez, J. J., Prince, G. M., Okada, H., Lachmann, P. J., and Medof, M. E. (1992) Structural properties of the glycoplasmanylinositol anchor phospholipid of the complement membrane attack complex inhibitor CD59. Clin. Exp. Immunol. 87, 415-421
50. Old, W. M., Shabb, J. B., Houel, S., Wang, H., Couts, K. L., Yen, C. Y., Litman, E. S., Croy, C. H., Meyer-Arendt, K., Miranda, J. G., Brown, R. A., Witze, E. S., Schweppe, R. E., Resing, K. A., and Ahn, N. G. (2009) Functional proteomics identifies targets of phosphorylation by B-Raf signaling in melanoma. Mol. Cell 34, 115-131
51. Palmisano, G., Melo-Braga, M. N., Engholm-Keller, K., Parker, B. L., and Larsen, M. R. (2012) Chemical deamidation: a common pitfall in largescale N-linked glycoproteomic mass spectrometry-based analyses. J. Proteome Res. 11, 1949-1957
52. Szklarczyk, D., Franceschini, A., Kuhn, M., Simonovic, M., Roth, A., Minguez, P., Doerks, T., Stark, M., Muller, J., Bork, P., Jensen, L. J., and von Mering, C. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39, D561-D568
53. Humphries, M. J., Obara, M., Olden, K., and Yamada, K. M. (1989) Role of fibronectin in adhesion, migration, and metastasis. Cancer Invest. 7, 373-393
54. Hynes, R. O., and Yamada, K. M. (1982) Fibronectins: multifunctional modular glycoproteins. J. Cell Biol. 95, 369-377
55. Yamada, K. M. (1991) Adhesive recognition sequences. J. Biol. Chem. 266, 12809-12812
56. George, E. L., Georges-Labouesse, E. N., Patel-King, R. S., Rayburn, H., and Hynes, R. O. (1993) Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119, 1079-1091
57. Price, J., and Hynes, R. O. (1985) Astrocytes in culture synthesize and secrete a variant form of fibronectin. J. Neurosci. 5, 2205-2211
58. Igakura, T., Kadomatsu, K., Kaname, T., Muramatsu, H., Fan, Q. W., Miyauchi, T., Toyama, Y., Kuno, N., Yuasa, S., Takahashi, M., Senda, T., Taguchi, O., Yamamura, K., Arimura, K., and Muramatsu, T. (1998) A null mutation in basigin, an immunoglobulin superfamily member, indicates its important roles in peri-implantation development and spermatogenesis. Dev. Biol. 194, 152-165
59. Kirk, P., Wilson, M. C., Heddle, C., Brown, M. H., Barclay, A. N., and Halestrap, A. P. (2000) CD147 is tightly associated with lactate transporters MCT1 and MCT4 and facilitates their cell surface expression. EMBO J. 19, 3896-3904
60. Muramatsu, T., and Miyauchi, T. (2003) Basigin (CD147): a multifunctional transmembrane protein involved in reproduction, neural function, inflammation and tumor invasion. Histol. Histopathol. 18, 981-987
61. Adewumi, O., Aflatoonian, B., Ahrlund-Richter, L., Amit, M., Andrews, P. W., Beighton, G., Bello, P. A., Benvenisty, N., Berry, L. S., Bevan, S., Blum, B., Brooking, J., Chen, K. G., Choo, A. B., Churchill, G. A., Corbel, M., Damjanov, I., Draper, J. S., Dvorak, P., Emanuelsson, K., Fleck, R. A., Ford, A., Gertow, K., Gertsenstein, M., Gokhale, P. J., Hamilton, R. S., Hampl, A., Healy, L. E., Hovatta, O., Hyllner, J., Imreh, M. P., Itskovitz-Eldor, J., Jackson, J., Johnson, J. L., Jones, M., Kee, K., King, B. L., Knowles, B. B., Lako, M., Lebrin, F., Mallon, B. S., Manning, D., Mayshar, Y., McKay, R. D., Michalska, A. E., Mikkola, M., Mileikovsky, M., Minger, S. L., Moore, H. D., Mummery, C. L., Nagy, A., Nakatsuji, N., O'Brien, C. M., Oh, S. K., Olsson, C., Otonkoski, T., Park, K. Y., Passier, R., Patel, H., Patel, M., Pedersen, R., Pera, M. F., Piekarczyk, M. S., Pera, R. A., Reubinoff, B. E., Robins, A. J., Rossant, J., Rugg-Gunn, P., Schulz, T. C., Semb, H., Sherrer, E. S., Siemen, H., Stacey, G. N., Stojkovic, M., Suemori, H., Szatkiewicz, J., Turetsky, T., Tuuri, T., van den Brink, S., Vintersten, K., Vuoristo, S., Ward, D., Weaver, T. A., Young, L. A., and Zhang, W. (2007) Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat. Biotechnol. 25, 803-816
62. Arimura, N., and Kaibuchi, K. (2007) Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat. Rev. Neurosci. 8, 194-205
63. Akama, K., Horikoshi, T., Nakayama, T., Otsu, M., Imaizumi, N., Nakamura, M., Toda, T., Inuma, M., Hirano, H., Kondo, Y., Suzuki, Y., and Inoue, N. (2011) Proteomic identification of differentially expressed genes in neural stem cells and neurons differentiated from embryonic stem cells of cynomolgus monkey (Macaca fascicularis) in vitro. Biochim. Biophys. Acta 1814, 265-276
64. Maurer, M. H., Feldmann, R. E., Jr., Futterer, C. D., Butlin, J., and Kuschinsky, W. (2004) Comprehensive proteome expression profiling of undifferentiated versus differentiated neural stem cells from adult rat hippocampus. Neurochem. Res. 29, 1129-1144
65. Eaton, B. A., Fetter, R. D., and Davis, G. W. (2002) Dynactin is necessary for synapse stabilization. Neuron 34, 729-741
66. Chang, H. P., Lindberg, F. P., Wang, H. L., Huang, A. M., and Lee, E. H. (1999) Impaired memory retention and decreased long-term potentiation in integrin-associated protein-deficient mice. Learn Mem. 6, 448-457
67. Koshland, D. E., Jr., Walsh, K., and LaPorte, D. C. (1985) Sensitivity of metabolic fluxes to covalent control. Curr. Top Cell Regul. 27, 13-22
68. Le Belle, J. E., Orozco, N. M., Paucar, A. A., Saxe, J. P., Mottahedeh, J., Pyle, A. D., Wu, H., and Kornblum, H. I. (2011) Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 8, 59-71
69. Poli, G., Leonarduzzi, G., Biasi, F., and Chiarpotto, E. (2004) Oxidative stress and cell signalling. Curr. Med. Chem. 11, 1163-1182
70. Wyss, M., and Kaddurah-Daouk, R. (2000) Creatine and creatinine metabolism. Physiol. Rev. 80, 1107-1213
71. Dirks, P., Thomas, U., and Montag, D. (2006) The cytoplasmic domain of NrCAM binds to PDZ domains of synapse-associated proteins SAP90/ PSD95 and SAP97. Eur. J. Neurosci. 24, 25-31
72. Doliana, R., Mongiat, M., Bucciotti, F., Giacomello, E., Deutzmann, R., Volpin, D., Bressan, G. M., and Colombatti, A. (1999) EMILIN, a component of the elastic fiber and a new member of the C1q/tumor necrosis factor superfamily of proteins. J. Biol. Chem. 274, 16773-16781
73. Braghetta, P., Ferrari, A., de Gemmis, P., Zanetti, M., Volpin, D., Bonaldo, P., and Bressan, G. M. (2002) Expression of the EMILIN-1 gene during mouse development. Matrix Biol. 21, 603-609
74. Kikkawa, U., Matsuzaki, H., and Yamamoto, T. (2002) Protein kinase C delta (PKC delta): activation mechanisms and functions. J. Biochem. 132, 831-839
75. Payne, D. M., Rossomando, A. J., Martino, P., Erickson, A. K., Her, J. H., Shabanowitz, J., Hunt, D. F., Weber, M. J., and Sturgill, T. W. (1991) Identification of the regulatory phosphorylation sites in pp42/mitogenactivated protein kinase (MAP kinase). EMBO J. 10, 885-892
76. Cheng, M., Zhen, E., Robinson, M. J., Ebert, D., Goldsmith, E., and Cobb, M. H. (1996) Characterization of a protein kinase that phosphorylates serine 189 of the mitogen-activated protein kinase homolog ERK3. J. Biol. Chem. 271, 12057-12062
77. Seger, R., and Krebs, E. G. (1995) The MAPK signaling cascade. FASEB J. 9, 726-735
78. Armstrong, L., Hughes, O., Yung, S., Hyslop, L., Stewart, R., Wappler, I., Peters, H., Walter, T., Stojkovic, P., Evans, J., Stojkovic, M., and Lako, M. (2006) The role of PI3K/AKT, MAPK/ERK and NFkappabeta signalling in the maintenance of human embryonic stem cell pluripotency and viability highlighted by transcriptional profiling and functional analysis. Hum. Mol. Genet. 15, 1894-1913
79. Wang, B., Gao, Y., Xiao, Z., Chen, B., Han, J., Zhang, J., Wang, X., and Dai, J. (2009) Erk1/2 promotes proliferation and inhibits neuronal differentiation of neural stem cells. Neurosci. Lett. 461, 252-257
80. Chao, A., Zhang, X., Ma, D., Langlais, P., Luo, M., Mandarino, L. J., Zingsheim, M., Pham, K., Dillon, J., and Yi, Z. (2012) Site-specific phosphorylation of protein phosphatase 1 regulatory subunit 12A stimulated or suppressed by insulin. J Proteomics 75, 3342-3350
81. Adams, J. A. (2001) Kinetic and catalytic mechanisms of protein kinases. Chem. Rev. 101, 2271-2290
82. Colbran, R. J., and Soderling, T. R. (1990) Calcium/calmodulin-dependent protein kinase II. Curr. Top Cell Regul. 31, 181-221
83. Linding, R., Jensen, L. J., Ostheimer, G. J., van Vugt, M. A., Jorgensen, C., Miron, I. M., Diella, F., Colwill, K., Taylor, L., Elder, K., Metalnikov, P., Nguyen, V., Pasculescu, A., Jin, J., Park, J. G., Samson, L. D., Woodgett, J. R., Russell, R. B., Bork, P., Yaffe, M. B., and Pawson, T. (2007) Systematic discovery of in vivo phosphorylation networks. Cell 129, 1415-1426
84. Yanagisawa, M., and Yu, R. K. (2007) The expression and functions of glycoconjugates in neural stem cells. Glycobiology 17, 57R-74R
85. Couchman, J. R. (2010) Transmembrane signaling proteoglycans. Annu. Rev. Cell Dev. Biol. 26, 89-114
86. Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R. C., and Melton, D. A. (2002) "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298, 597-600
87. Hall, P. E., Lathia, J. D., Caldwell, M. A., and Ffrench-Constant, C. (2008) Laminin enhances the growth of human neural stem cells in defined culture media. BMC Neurosci 9, 71
88. Oh, E. S., Couchman, J. R., and Woods, A. (1997) Serine phosphorylation of syndecan-2 proteoglycan cytoplasmic domain. Arch. Biochem. Biophys. 344, 67-74
89. Boroviak, T., and Rashbass, P. (2011) The apical polarity determinant Crumbs 2 is a novel regulator of ESC-derived neural progenitors. Stem Cells 29, 193-205
90. Banziger, C., Soldini, D., Schutt, C., Zipperlen, P., Hausmann, G., and Basler, K. (2006) Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell 125, 509-522
91. Bartscherer, K., Pelte, N., Ingelfinger, D., and Boutros, M. (2006) Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 125, 523-533
92. Sato, N., Meijer, L., Skaltsounis, L., Greengard, P., and Brivanlou, A. H. (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 10, 55-63
93. Willert, K., Brown, J. D., Danenberg, E., Duncan, A. W., Weissman, I. L., Reya, T., Yates, J. R., 3rd, and Nusse, R. (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448-452
94. Nusse, R. (2008) Wnt signaling and stem cell control. Cell Res. 18, 523-527
95. Kalani, M. Y., Cheshier, S. H., Cord, B. J., Bababeygy, S. R., Vogel, H., Weissman, I. L., Palmer, T. D., and Nusse, R. (2008) Wnt-mediated self-renewal of neural stem/progenitor cells. Proc. Natl. Acad. Sci. U.S.A. 105, 16970-16975
96. Lange, C., Mix, E., Rateitschak, K., and Rolfs, A. (2006) Wnt signal pathways and neural stem cell differentiation. Neurodegener. Dis. 3, 76-86
97. Muroyama, Y., Kondoh, H., and Takada, S. (2004) Wnt proteins promote neuronal differentiation in neural stem cell culture. Biochem. Biophys. Res. Commun. 313, 915-921
98. Lie, D. C., Colamarino, S. A., Song, H. J., Desire, L., Mira, H., Consiglio, A., Lein, E. S., Jessberger, S., Lansford, H., Dearie, A. R., and Gage, F. H. (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437, 1370-1375
99. Herz, J., Clouthier, D. E., and Hammer, R. E. (1992) LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell 71, 411-421
100. May, P., Rohlmann, A., Bock, H. H., Zurhove, K., Marth, J. D., Schomburg, E. D., Noebels, J. L., Beffert, U., Sweatt, J. D., Weeber, E. J., and Herz, J. (2004) Neuronal LRP1 functionally associates with postsynaptic proteins and is required for normal motor function in mice. Mol. Cell. Biol. 24, 8872-8883