Temporal analysis of neural differentiation using quantitative proteomics

Journal of Proteome Research

Volumn 8, Issue 3, 2009, Pages 1315-1326

  Chaerkady, Raghothama ^a,b   Kerr, Candace L ^b   Marimuthu, Arivusudar ^a,b   Kelkar, Dhanashree S ^a   Kashyap, Manoj Kumar ^a,b   Gucek, Marjan ^b   Gearhart, John D ^b   Pandey, Akhilesh ^a,b  

^a Institute of Bioinformatics   (India)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytes; Embryonic stem cells; ITRAQ; Motor neurons; Proteomic profiling

Indexed keywords

ALKALINE PHOSPHATASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE I; CELLULAR RETINOIC ACID BINDING PROTEIN 2; DOUBLECORTIN; FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 5; GLYCOGEN PHOSPHORYLASE; HEAT SHOCK PROTEIN 27; KARYOPHERIN; NESTIN; NEUROFILAMENT M PROTEIN; PROTEIN S 100; RETINOIC ACID BINDING PROTEIN; SPECTRIN; TENASCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DOWN REGULATION; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; ISOBARIC TAG FOR RELATIVE AND ABSOLUTE QUANTITATION; MOTONEURON; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; TANDEM MASS SPECTROMETRY; UPREGULATION; WESTERN BLOTTING;

ANTIGENS, DIFFERENTIATION; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; HUMANS; NEUROGENESIS; PROTEOME;

EID: 65249167537     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr8006667     Document Type: Article

References (45)

1. Smukler, S. R.; Runciman, S. B.; Xu, S.; van der Kooy, D. Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences. J. Cell Biol. 2006, 172 (1), 79-90.
2. Vallier, L.; Rugg-Gunn, P. J.; Bouhon, I. A.; Andersson, F. K.; Sadler, A. J.; Pedersen, R. A. Enhancing and diminishing gene function in human embryonic stem cells. Stem Cells 2004, 22 (1), 2-11.
3. ThomsonJ. A. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282 (5391) 1145-1147 [erratum appears in Science 1998 282 (5395) 1827].
4. Reubinoff, B. E.; Pera, M. F.; Fong, C. Y.; Trounson, A.; Bongso, A. Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat. Biotechnol. 2000, 18 (4), 399-404.
5. Shin, S.; Sun, Y.; Liu, Y.; Khaner, H.; Svant, S.; Cai, J.; Xu, Q. X.; Davidson, B. P.; Stice, S. L.; Smith, A. K.; Goldman, S. A.; Reubinoff, B. E.; Zhan, M.; Rao, M. S.; Chesnut, J. D. Whole genome analysis of human neural stem cells derived from embryonic stem cells and stem and progenitor cells isolated from fetal tissue. Stem Cells 2007, 25 (5), 1298-1306.
6. Cheng, L.; Sung, M. T.; Cossu-Rocca, P.; Jones, T. D.; MacLennan, G. T.; De Jong, J.; Lopez-Beltran, A.; Montironi, R.; Looijenga, L. H. OCT4: biological functions and clinical applications as a marker of germ cell neoplasia. J. Pathol. 2007, 211 (1), 1-9.
7. Lee, H.; Shamy, G. A.; Elkabetz, Y.; Schofield, C. M.; Harrsion, N. L.; Panagiotakos, G.; Socci, N. D.; Tabar, V.; Studer, L. Directed differentiation and transplantation of human embryonic stem cell- derived motoneurons. Stem Cells 2007, 25 (8), 1931-1939.
8. Wu, H.; Xu, J.; Pang, Z. P.; Ge, W.; Kim, K. J.; Blanchi, B.; Chen, C.; Sudhof, T. C.; Sun, Y. E. Integrative genomic and functional analyses reveal neuronal subtype differentiation bias in human embryonic stem cell lines. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (34), 13821-13826.
9. Zhong, J. F.; Song, Y.; Du, J.; Gamache, C.; Burke, K. A.; Lund, B. T.; Weiner, L. P. Gene regulation networks related to neural differentiation of hESC. Gene Expression 2007, 14 (1), 23-34.
10. Van Hoof, D.; Passier, R.; Ward-Van Oostwaard, D.; Pinkse, M. W.; Heck, A. J.; Mummery, C. L.; Krijgsveld, J. A quest for human and mouse embryonic stem cell-specific proteins. Mol. Cell. Proteomics 2006, 5 (7), 1261-1273.
11. Van Hoof, D.; Mummery, C. L.; Heck, A. J.; Krijgsveld, J. Embryonic stem cell proteomics. Expert Rev. Proteomics 2006, 3 (4), 427-437.
12. Baharvand, H.; Hajheidari, M.; Ashtiani, S. K.; Salekdeh, G. H. Proteomic signature of human embryonic stem cells. Proteomics 2006, 6 (12), 3544-3549.
13. Yocum, A. K.; Gratsch, T. E.; Leff, N.; Strahler, J. R.; Hunter, C. L.; Walker, A. K.; Michailidis, G.; Omenn, G. S.; O'Shea, K. S.; Andrews, P. C. Coupled global and targeted proteomics of human embryonic stem cells during induced differentiation. Mol. Cell. Proteomics 2008, 7 (4), 750-767.
14. Ideker, T.; Thorsson, V.; Ranish, J. A.; Christmas, R.; Buhler, J.; Eng, J. K.; Bumgarner, R.; Goodlett, D. R.; Aebersold, R.; Hood, L. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 2001, 292 (5518), 929-934.
15. Tian, G. W.; Mohanty, A.; Chary, S. N.; Li, S.; Paap, B.; Drakakaki, G.; Kopec, C. D.; Li, J.; Ehrhardt, D.; Jackson, D.; Rhee, S. Y.; Raikhel, N. V.; Citovsky, V. High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol. 2004, 135 (1), 25-38.
16. Choe, L.; D'Ascenzo, M.; Relkin, N. R.; Pappin, D.; Ross, P.; Williamson, B.; Guertin, S.; Pribil, P.; Lee, K. H. 8-plexquantitation of changes in cerebrospinal fluid protein expression in subjects undergoing intravenous immunoglobulin treatment for Alzheimer's disease. Proteomics 2007, 7 (20), 3651-3660.
17. Ow, S. Y.; Cardona, T.; Taton, A.; Magnuson, A.; Lindblad, P.; Stensjo, K.; Wright, P. C. Quantitative shotgun proteomics of enriched heterocysts from Nostoc sp. PCC 7120 using 8-plex isobaric peptide tags. J. Proteome Res. 2008, 7 (4), 1615-1628.
18. Bottenstein, J. E.; Sato, G. H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. U.S.A. 1979, 76 (1), 514-517.
19. Sterneckert, J. L.; Hill, C. M.; Palmer, R.; Gearhart, J. D. Bone morphogenetic proteins produced by cells within embryoid bodies inhibit ventral directed differentiation by Sonic Hedgehog. Cloning Stem Cells 2005, 7 (1), 27-34.
20. Draper, J. S.; Pigott, C.; Thomson, J. A.; Andrews, P. W. Surface antigens of human embryonic stem cells: changes upon differentiation in culture. J. Anat. 2002, 200 (Pt 3), 249-258.
21. Winger, Q. A.; Guttormsen, J.; Gavin, H.; Bhushan, F. Heat shock protein 1 and the mitogen-activated protein kinase 14 pathway are important for mouse trophoblast stem cell differentiation. Biol. Reprod. 2007, 76 (5), 884-891.
22. Fukada, Y.; Yasui, K.; Kitayama, M.; Doi, K.; Nakano, T.; Watanabe, Y.; Nakashima, K. Gene expression analysis of the murine model of amyotrophic lateral sclerosis: studies of the Leu126delTT mutation in SOD1. Brain Res. 2007, 1160, 1-10.
23. Yasuhara, N.; Shibazaki, N.; Tanaka, S.; Nagai, M.; Kamikawa, Y.; Oe, S.; Asally, M.; Kamachi, Y.; Kondoh, H.; Yoneda, Y. Triggering neural differentiation of ES cells by subtype switching of importinalpha. Nat. Cell Biol. 2007, 9 (1), 72-79.
24. Wrage, P. C.; Tran, T.; To, K.; Keefer, E. W.; Ruhn, K. A.; Hong, J.; Hattangadi, S.; Trevino, I.; Tansey, M. G. The neuro-glial properties of adipose-derived adult stromal (ADAS) cells are not regulated by Notch 1 and are not derived from neural crest lineage. PLoS One 2008, 3 (1), e1453.
25. Li, J. Y.; Pu, M. T.; Hirasawa, R.; Li, B. Z.; Huang, Y. N.; Zeng, R.; Jing, N. H.; Chen, T.; Li, E.; Sasaki, H.; Xu, G. L. Synergistic function of DNA methyltransferases Dnmt3a and Dnmt3b in the methylation of Oct4 and Nanog. Mol. Cell. Biol. 2007, 27 (24), 8748-8759.
26. Liu, Y. L.; Guo, Y. S.; Xu, L.; Wu, S. Y.; Wu, D. X.; Yang, C.; Zhang, Y.; Li, C. Y. Alternation of neurofilaments in immune-mediated injury of spinal cord motor neurons. Spinal Cord 2008, in press
27. Perrot, R.; Berges, R.; Bocquet, A.; Eyer, J. Review of the multiple aspects of neurofilament functions, and their possible contribution to neurodegeneration. Mol. Neurobiol. 2008, 38 (1), 27-65.
28. Brady, S. T. Motor neurons and neurofilaments in sickness and in health. Cell 1993, 73 (1), 1-3.
29. Crossin, K. L.; Hoffman, S.; Tan, S. S.; Edelman, G. M. Cytotactin and its proteoglycan ligand mark structural and functional boundaries in somatosensory cortex of the early postnatal mouse. Dev. Biol. 1989, 136 (2), 381-392.
30. Irintchev, A.; Rollenhagen, A.; Troncoso, E.; Kiss, J. Z.; Schachner, M. Structural and functional aberrations in the cerebral cortex of tenascin-C deficient mice. Cereb. Cortex 2005, 15 (7), 950-962.
31. Ikeshima-Kataoka, H.; Saito, S.; Yuasa, S. Tenascin-C is required for proliferation of astrocytes in primary culture. In Vivo 2007, 21 (4), 629-633.
32. Witusik, M.; Piaskowski, S.; Hulas-Bigoszewska, K.; Zakrzewska, M.; Gresner, S. M.; Azizi, S. A.; Krynska, B.; Liberski, P. P.; Rieske, P. Successful elimination of non-neural cells and unachievable elimination of glial cells by means of commonly used cell culture manipulations during differentiation of GFAP and SOX2 positive neural progenitors (NHA) to neuronal cells. BMC Biotechnol. 2008, 8, 56.
33. Kose, N.; Asashima, T.; Muta, M.; Iizasa, H.; Sai, Y.; Terasaki, T.; Nakashima, E. Altered expression of basement membrane-related molecules in rat brain pericyte, endothelial, and astrocyte cell lines after transforming growth factor-beta1 treatment. Drug Metab. Pharmacokinet. 2007, 22 (4), 255-266.
34. Chan-Ling, T.; Chu, Y.; Baxter, L.; Weible Ii, M.; Hughes, S. In vivo characterization of astrocyte precursor cells (APCs) and astrocytes in developing rat retinae: Differentiation, proliferation, and apoptosis. Glia 2008, 57 (1), 39-53.
35. Pekny, M.; Wilhelmsson, U.; Bogestal, Y. R.; Pekna, M. The role of astrocytes and complement system in neural plasticity. Int. Rev. Neurobiol. 2007, 82, 95-111.
36. Feral, C. C.; Zijlstra, A.; Tkachenko, E.; Prager, G.; Gardel, M. L.; Slepak, M.; Ginsberg, M. H. CD98hc (SLC3A2) participates in fibronectin matrix assembly by mediating integrin signaling. J. Cell Biol. 2007, 178 (4), 701-711.
37. Kim, J. Y.; Wu, Y.; Smas, C. M. Characterization of ScAP-23, a new cell line from murine subcutaneous adipose tissue, identifies genes for the molecular definition of preadipocytes. Physiol. Genomics 2007, 31 (2), 328-342.
38. Salim, K.; Kehoe, L.; Minkoff, M. S.; Bilsland, J. G.; Munoz-Sanjuan, I.; Guest, P. C. Identification of differentiating neural progenitor cell markers using shotgun isobaric tagging mass spectrometry. Stem Cells Dev. 2006, 15 (3), 461-470.
39. Scaturro, M.; Cestelli, A.; Castiglia, D.; Nastasi, T.; Di Liegro, I. Posttranscriptional regulation of H1 zero and H3.3B histone genes in differentiating rat cortical neurons. Neurochem. Res. 1995, 20 (8), 969-976.
40. Sarkar, S. A.; Sharma, R. P. Expression of selected apoptosis related genes, MIF, IGIF and TNF alpha, during retinoic acid-induced neural differentiation in murine embryonic stem cells. Cell Struct. Funct. 2002, 27 (2), 99-107.
41. Molina, H.; Yang, Y.; Ruch, T.; Kim, J. W.; Mortensen, P.; Otto, T.; Nalli, A.; Tang, Q. Q.; Lane, M. D.; Chaerkady, R.; Pandey, A. Temporal profiling of the adipocyte proteome during differentiation using a five-plex SILAC based strategy. J. Proteome Res. 2009, 8 (1), 48-58.
42. Battista, S.; Pentimalli, F.; Baldassarre, G.; Fedele, M.; Fidanza, V.; Croce, C. M.; Fusco, A. Loss of Hmga1 gene function affects embryonic stem cell lympho-hematopoietic differentiation. FASEB J. 2003, 17 (11), 1496-1498.
43. Liang, J.; Wan, M.; Zhang, Y.; Gu, P.; Xin, H.; Jung, S. Y.; Qin, J.; Wong, J.; Cooney, A. J.; Liu, D.; Songyang, Z. Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat. Cell Biol. 2008, 10 (6), 731-739.
44. Maldonado-Saldivia, J.; van den Bergen, J.; Krouskos, M.; Gilchrist, M.; Lee, C.; Li, R.; Sinclair, A. H.; Surani, M. A.; Western, P. S. Dppa and Dppa4 are closely linked SAP motif genes restricted to pluripotent cells and the germ line. Stem Cells 2007, 25 (1), 1928.
45. Mathivanan, S.; Ahmed, M.; Ahn, N. G.; Alexandre, H.; Amanchy, R.; Andrews, P. C.; Bader, J. S.; Balgley, B. M.; Bantscheff, M.; Bennett, K. L.; Bjorling, E.; Blagoev, B.; Bose, R.; Brahmachari, S. K.; Burlingame, A. S.; Bustelo, X. R.; Cagney, G.; Cantin, G. T.; Cardasis, H. L.; Celis, J. E.; Chaerkady, R.; Chu, F.; Cole, P. A.; Costello, C. E.; Cotter, R. J.; Crockett, D.; DeLany, J. P.; De Marzo, A. M.; DeSouza, L. V.; Deutsch, E. W.; Dransfield, E.; Drewes, G.; Droit, A.; Dunn, M. J.; Elenitoba-Johnson, K.; Ewing, R. M.; Van Eyk, J.; Faca, V.; Falkner, J.; Fang, X.; Fenselau, C.; Figeys, D.; Gagne, P.; Gelfi, C.; Gevaert, K.; Gimble, J. M.; Gnad, F.; Goel, R.; Gromov, P.; Hanash, S. M.; Hancock, W. S.; Harsha, H. C.; Hart, G.; Hays, F.; He, F.; Hebbar, P.; Helsens, K.; Hermeking, H.; Hide, W.; Hjerno, K.; Hochstrasser, D. F.; Hofmann, O.; Horn, D. M.; Hruban, R. H.; Ibarrola, N.; James, P.; Jensen, O. N.; Jensen, P. H.; Jung, P.; Kandasamy, K.; Kheterpal, I.; Kikuno, R. F.; Korf, U.; Korner, R.; Kuster, B.; Kwon, M. S.; Lee, H. J.; Lee, Y. J.; Lefevre, M.; Lehvaslaiho, M.; Lescuyer, P.; Levander, F.; Lim, M. S.; Lobke, C.; Loo, J. A.; Mann, M.; Martens, L.; Martinez-Heredia, J.; McComb, M.; McRedmond, J.; Mehrle, A.; Menon, R.; Miller, C. A.; Mischak, H.; Mohan, S. S.; Mohmood, R.; Molina, H.; Moran, M. F.; Morgan, J. D.; Moritz, R.; Morzel, M.; Muddiman, D. C.; Nalli, A.; Navarro, J. D.; Neubert, T. A.; Ohara, O.; Oliva, R.; Omenn, G. S.; Oyama, M.; Paik, Y. K.; Pennington, K.; Pepperkok, R.; Periaswamy, B.; Petricoin, E. F.; Poirier, G. G.; Prasad, T. S.; Purvine, S. O.; Rahiman, B. A.; Ramachandran, P.; Ramachandra, Y. L.; Rice, R. H.; Rick, J.; Ronnholm, R. H.; Salonen, J.; Sanchez, J. C.; Sayd, T.; Seshi, B.; Shankari, K.; Sheng, S. J.; Shetty, V.; Shivakumar, K.; Simpson, R. J.; Sirdeshmukh, R.; Siu, K. W.; Smith, J. C.; Smith, R. D.; States, D. J.; Sugano, S.; Sullivan, M.; uperti-Furga, G.; Takatalo, M.; Thong- boonkerd, V.; Trinidad, J. C.; Uhlen, M.; Vandekerckhove, J.; Vasilescu, J.; Veenstra, T. D.; Vidal-Taboada, J. M.; Vihinen, M.; Wait, R.; Wang, X.; Wiemann, S.; Wu, B.; Xu, T.; Yates, J. R.; Zhong, J.; Zhou, M.; Zhu, Y.; Zurbig, P.; Pandey, A. Human Proteinpedia enables sharing of human protein data. Nat. Biotechnol. 2008, 26 (2), 164-167.