New insights in osteogenic differentiation revealed by mass spectrometric assessment of phosphorylated substrates in murine skin mesenchymal cells

BMC Cell Biology

Volumn 14, Issue 1, 2013, Pages

  Halcsik, Erik ^a   Forni, Maria F ^a   Fujita, Andre ^a   Verano Braga, Thiago ^b   Jensen, Ole N ^b   Sogayar, Mari C ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; CASEIN KINASE; CYCLIN DEPENDENT KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHOTRANSFERASE; RAS PROTEIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; WNT PROTEIN;

ARTICLE; BIOINFORMATICS; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; GENE REARRANGEMENT; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MESENCHYMAL STEM CELL; OSTEOBLAST; PROTEIN DATABASE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION;

MURINAE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CASEIN KINASES; CELL DIFFERENTIATION; CYCLIN-DEPENDENT KINASES; GENE EXPRESSION REGULATION; MAP KINASE KINASE 4; MASS SPECTROMETRY; MESENCHYMAL STROMAL CELLS; MICE; OSTEOBLASTS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOPROTEINS; PHOSPHORYLATION; RAS PROTEINS; SIGNAL TRANSDUCTION; SKIN; WNT PROTEINS;

EID: 84886936036     PISSN: None     EISSN: 14712121     Source Type: Journal    
DOI: 10.1186/1471-2121-14-47     Document Type: Article

References (62)

1. Deschaseaux F, Sensébé L, Heymann D. Mechanisms of bone repair and regeneration. Trends Mol Med 2009, 15:417-429. 10.1016/j.molmed.2009.07.002, 19740701.
2. Deschaseaux F, Pontikoglou C, Sensebe L. Bone regeneration: the stem/progenitor cells point of view. J Cell Mol Med 2010, 14:103-115. 10.1111/j.1582-4934.2009.00878.x, 19840188.
3. García-Castro J, Trigueros C, Madrenas J, Pérez-Simón JA, Rodriguez R, Menendez P. Mesenchymal stem cells and their use as cell replacement therapy and disease modelling tool. J Cell Mol Med 2008, 12:2552-2565. 10.1111/j.1582-4934.2008.00516.x, 19210755.
4. Driskell RR, Clavel C, Rendl M, Watt FM. Hair follicle dermal papilla cells at a glance. J Cell Sci 2011, 124(Pt 8):1179-1182. 3115771, 21444748.
5. Vaculik C, Schuster C, Bauer W, Iram N, Pfisterer K, Kramer G, Reinisch A, Strunk D, Elbe-Bürger A. Human dermis harbors distinct mesenchymal stromal cell subsets. J Invest Dermatol 2011, 132(3 Pt 1):563-74. 3278768, 22048731.
6. Fuentealba LC, Eivers E, Ikeda A, Hurtado C, Kuroda H, Pera EM, De Robertis EM. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 2007, 131:980-993. 10.1016/j.cell.2007.09.027, 2200633, 18045539.
7. Boersema PJ, Mohammed S, Heck AJR. Phosphopeptide fragmentation and analysis by mass spectrometry. J Mass Spectrom Jms 2009, 44:861-878.
8. Jensen ON. Interpreting the protein language using proteomics. Nat Rev Mol Cell Biol 2006, 7:391-403. 10.1038/nrm1939, 16723975.
9. Larsen MR, Trelle MB, Thingholm TE, Jensen ON. Analysis of posttranslational modifications of proteins by tandem mass spectrometry. Biotechniques 2006, 40:790-798. 10.2144/000112201, 16774123.
10. Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jorgensen TJ. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol Cell Proteomics 2005, 4:873-886. 10.1074/mcp.T500007-MCP200, 15858219.
11. Posewitz MC, Tempst P. Immobilized gallium(III) affinity chromatography of phosphopeptides. Anal Chem 1999, 71:2883-2892. 10.1021/ac981409y, 10424175.
12. Hsu J-L, Huang S-Y, Chow N-H, Chen S-H. Stable-isotope dimethyl labeling for quantitative proteomics. Anal Chem 2003, 75:6843-52. 10.1021/ac0348625, 14670044.
13. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S, Heck AJ. Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 2009, 4:484-494. 10.1038/nprot.2009.21, 19300442.
14. Steen H, Jebanathirajah JA, Rush J, Morrice N, Kirschner MW. Phosphorylation analysis by mass spectrometry: myths, facts, and the consequences for qualitative and quantitative measurements. Mol Cell Proteomics 2006, 5:172-181.
15. Savitski MM, Lemeer S, Boesche M, Lang M, Mathieson T, Bantscheff M, Kuster B. Confident phosphorylation site localization using the Mascot Delta Score. Mol Cell proteomics MCP 2011, 10:M110.003830.
16. Vlieghe D, Sandelin A, De Bleser PJ, Vleminckx K, Wasserman WW, Van Roy F, Lenhard B. A new generation of JASPAR, the open-access repository for transcription factor binding site profiles. Nucleic Acids Res 2006, 34(Database issue):D95-D97. 1347477, 16381983.
17. Schneider TD, Stephens RM. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 1990, 18:6097-6100. 10.1093/nar/18.20.6097, 332411, 2172928.
18. Stormo GD. DNA binding sites: representation and discovery. Bioinformatics 2000, 16:16-23. 10.1093/bioinformatics/16.1.16, 10812473.
19. Wasserman WW, Sandelin A. Applied bioinformatics for the identification of regulatory elements. Nat Rev Genet 2004, 5:276-287. 10.1038/nrg1315, 15131651.
20. Robertson G, Bilenky M, Lin K, He A, Yuen W, Dagpinar M, Varhol R, Teague K, Griffith OL, Zhang X, Pan Y, Hassel M, Sleumer MC, Pan W, Pleasance ED, Chuang M, Hao H, Li YY, Robertson N, Fjell C, Li B, Montgomery SB, Astakhova T, Zhou J, Sander J, Siddiqui AS, Jones SJM. cisRED: a database system for genome-scale computational discovery of regulatory elements. Nucleic Acids Res 2006, 34(Database issue):D68-D73. 1347438, 16381958.
21. Song CX, Wang FJ, Ye ML, Cheng K, Chen R, Zhu J, Tan YX, Wang HY, Figeys D, Zou HF. Improvement of the quantification accuracy and throughput for phosphoproteome analysis by a pseudo triplex stable isotope dimethyl labeling approach. Anal Chem 2011, 83:7755-7762. 10.1021/ac201299j, 21902226.
22. Balint E, Lapointe D, Drissi H, van der Meijden C, Young DW, van Wijnen AJ, Stein JL, Stein GS, Lian JB. Phenotype discovery by gene expression profiling: mapping of biological processes linked to BMP-2-mediated osteoblast differentiation. J Cell Biochem 2003, 89:401-426. 10.1002/jcb.10515, 12704803.
23. Ulsamer A, Ortuño MJ, Ruiz S, Susperregui ARG, Osses N, Rosa JL, Ventura F. BMP-2 induces Osterix expression through up-regulation of Dlx5 and its phosphorylation by p38. J Biol Chem 2008, 283:3816-26.
24. Quackenbush J. Computational analysis of microarray data. Nat Rev Genet 2001, 2:418-427. 10.1038/35076576, 11389458.
25. Cleveland WS. Robust locally-weighted regression and smoothing scatterplots. J Am Stat Assoc 1979, 74:829-836.
26. Fujita A, Sato JR, Rodrigues LDO, Ferreira CE, Sogayar MC. Evaluating different methods of microarray data normalization. BMC Bioinform 2006, 7:469.
27. Bragdon B, Thinakaran S, Moseychuk O, King D, Young K, Litchfield DW, Petersen NO, Nohe A. Casein kinase 2 beta-subunit is a regulator of bone morphogenetic protein 2 signaling. Biophys J 2010, 99:897-904. 10.1016/j.bpj.2010.04.070, 2913199, 20682268.
28. Bragdon B, Thinakaran S, Moseychuk O, Gurski L, Bonor J, Price C, Wang L, Beamer WG, Nohe A. Casein kinase 2 regulates in vivo bone formation through its interaction with bone morphogenetic protein receptor type Ia. Bone 2011, 49:944-54. 10.1016/j.bone.2011.06.037, 21763800.
29. Celil AB, Campbell PG. BMP-2 and insulin-like growth factor-I mediate Osterix (Osx) expression in human mesenchymal stem cells via the MAPK and protein kinase D signaling pathways. J Biol Chem 2005, 280:31353-9. 10.1074/jbc.M503845200, 16000303.
30. Huang Y, Lin J, Lin C, Su Y, Hung S. c-Jun N-Terminal Kinase 1 Negatively Regulates Osteoblastic Differentiation Induced by BMP-2 via Phosphorylation of Runx2 at Ser104. J Bone Miner Res 2012, 27:1093-105. 10.1002/jbmr.1548, 22247071.
31. Liu H, Liu Y, Viggeswarapu M, Zheng Z, Titus L, Boden SD. Activation of c-Jun NH(2)-terminal kinase 1 increases cellular responsiveness to BMP-2 and decreases binding of inhibitory Smad6 to the type 1 BMP receptor. J bone Miner Res Off J Am Soc Bone Miner Res 2011, 26:1122-1132.
32. Guicheux J, Lemonnier J, Ghayor C, Suzuki A, Palmer G, Caverzasio J. Activation of p38 mitogen-activated protein kinase and c-Jun-NH2-terminal kinase by BMP-2 and their implication in the stimulation of osteoblastic cell differentiation. J Bone Miner Res Off J Am Soc Bone Miner Res 2003, 18:2060-2068.
33. Bellosta P, Masramon L, Mansukhani A, Basilico C. p21(WAF1/CIP1) acts as a brake in osteoblast differentiation. J bone Miner Res Off J Am Soc Bone Miner Res 2003, 18:818-826.
34. Waters KM, Liu T, Quesenberry RD, Willse AR, Bandyopadhyay S, Kathmann LE, Weber TJ, Smith RD, Wiley HS, Thrall BD. Network analysis of epidermal growth factor signaling using integrated genomic. Proteomic and phosphorylation data. PLoS One 2012, 7:e34515. 10.1371/journal.pone.0034515, 3315547, 22479638.
35. Chen G, Deng C, Li YP. TGF-beta and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci 2012, 8:272-288. 3269610, 22298955.
36. Long F. Building strong bones: molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol 2011, 13:27-38. 10.1038/nrm3254, 22189423.
37. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89:755-764. 10.1016/S0092-8674(00)80258-5, 9182763.
38. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GW, Beddington RS, Mundlos S, Olsen BR, Selby PB, Owen MJ. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997, 89:765-771. 10.1016/S0092-8674(00)80259-7, 9182764.
39. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, De Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 2002, 108:17-29. 10.1016/S0092-8674(01)00622-5, 11792318.
40. Bi W, Deng JM, Zhang Z, Behringer RR, De Crombrugghe B. Sox9 is required for cartilage formation. Nat Genet 1999, 22:85-89. 10.1038/8792, 10319868.
41. Ducy P, Starbuck M, Priemel M, Shen J, Pinero G, Geoffroy V, Amling M, Karsenty G. A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development. Genes Dev 1999, 13:1025-1036. 10.1101/gad.13.8.1025, 316641, 10215629.
42. Guillot PV, De Bari C, Dell'Accio F, Kurata H, Polak J, Fisk NM. Comparative osteogenic transcription profiling of various fetal and adult mesenchymal stem cell sources. Differ Res Biol Divers 2008, 76:946-957.
43. Lindahl K, Barnes AM, Fratzl-Zelman N, Whyte MP, Hefferan TE, Makareeva E, Brusel M, Yaszemski MJ, Rubin C-J, Kindmark A, Roschger P, Klaushofer K, McAlister WH, Mumm S, Leikin S, Kessler E, Boskey AL, Ljunggren O, Marini JC. COL1 C-propeptide cleavage site mutations cause high bone mass osteogenesis imperfecta. Hum Mutat 2011, 32:598-609. 10.1002/humu.21475, 3103631, 21344539.
44. Bialek P, Kern B, Yang X, Schrock M, Sosic D, Hong N, Wu H, Yu K, Ornitz DM, Olson EN, Justice MJ, Karsenty G. A twist code determines the onset of osteoblast differentiation. Dev Cell 2004, 6:423-435. 10.1016/S1534-5807(04)00058-9, 15030764.
45. Bandyopadhyay A, Tsuji K, Cox K, Harfe BD, Rosen V, Tabin CJ. Genetic analysis of the roles of BMP2, BMP4, and BMP7 in limb patterning and skeletogenesis. PLoS Genet 2006, 2:15.
46. Robledo RF, Rajan L, Li X, Lufkin T. The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial, and appendicular skeletal development. Genes Dev 2002, 16:1089-1101. 10.1101/gad.988402, 186247, 12000792.
47. Lee M-H, Kim Y-J, Yoon W-J, Kim J-I, Kim B-G, Hwang Y-S, Wozney JM, Chi X-Z, Bae S-C, Choi K-Y, Cho J-Y, Choi J-Y, Ryoo H-M. Dlx5 specifically regulates Runx2 type II expression by binding to homeodomain-response elements in the Runx2 distal promoter. J Biol Chem 2005, 280:35579-87. 10.1074/jbc.M502267200, 16115867.
48. Rodríguez JP, González M, Ríos S, Cambiazo V. Cytoskeletal organization of human mesenchymal stem cells (MSC) changes during their osteogenic differentiation. J Cell Biochem 2004, 93:721-731. 10.1002/jcb.20234, 15660416.
49. Lo T, Tsai C-F, Shih Y-R V, Wang Y-T, Lu S-C, Sung T-Y, Hsu W-L, Chen Y-J, Lee OK. Phosphoproteomic analysis of human mesenchymal stromal cells during osteogenic differentiation. J Proteome Res 2012, 11:586-598. 10.1021/pr200868p, 22088210.
50. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 2004, 6:483-495. 10.1016/S1534-5807(04)00075-9, 15068789.
51. Shola DTN, Wang H, Wahdan-Alaswad R, Danielpour D. Hic-5 controls BMP4 responses in prostate cancer cells through interacting with Smads 1, 5 and 8. Oncogene 2011, 31:2480-2490. 3340512, 21996749.
52. Crigler L, Kazhanie A, Yoon T-J, Zakhari J, Anders J, Taylor B, Virador VM. Isolation of a mesenchymal cell population from murine dermis that contains progenitors of multiple cell lineages. FASEB J Off Publ Fed Am Soc Exp Biol 2007, 21:2050-2063.
53. Thingholm TE, Jensen ON, Robinson PJ, Larsen MR. SIMAC (sequential elution from IMAC), a phosphoproteomics strategy for the rapid separation of monophosphorylated from multiply phosphorylated peptides. Mol Cell Proteomics 2008, 7:661-671.
54. Gobom J, Nordhoff E, Mirgorodskaya E, Ekman R, Roepstorff P. Sample purification and preparation technique based on nano-scale reversed-phase columns for the sensitive analysis of complex peptide mixtures by matrix-assisted laser desorption/ionization mass spectrometry. J Mass Spectrom 1999, 34:105-116. 10.1002/(SICI)1096-9888(199902)34:2<105::AID-JMS768>3.0.CO;2-4, 10093212.
55. Beausoleil SA, Jedrychowski M, Schwartz D, Elias JE, Villen J, Li J, Cohn MA, Cantley LC, Gygi SP. Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci U S A 2004, 101:12130-12135. 10.1073/pnas.0404720101, 514446, 15302935.
56. Van Breukelen B, van den Toorn HW, Drugan MM, Heck AJ. StatQuant: a post-quantification analysis toolbox for improving quantitative mass spectrometry. Bioinformatics 2009, 25:1472-1473. 10.1093/bioinformatics/btp181, 19336442.
57. Linding R, Jensen LJ, Pasculescu A, Olhovsky M, Colwill K, Bork P, Yaffe MB, Pawson T. NetworKIN: a resource for exploring cellular phosphorylation networks. Nucleic Acids Res 2008, 36(Database issue):D695-D699. 2238868, 17981841.
58. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-6. 10.1093/bioinformatics/bti610, 16081474.
59. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009, 55:611-22. 10.1373/clinchem.2008.112797, 19246619.
60. Piek E, Sleumer LS, Van Someren EP, Heuver L, De Haan JR, De Grijs I, Gilissen C, Hendriks JM, Van Ravestein-van Os RI, Bauerschmidt S, Dechering KJ, Van Zoelen EJ. Osteo-transcriptomics of human mesenchymal stem cells: accelerated gene expression and osteoblast differentiation induced by vitamin D reveals c-MYC as an enhancer of BMP2-induced osteogenesis. Bone 2010, 46:613-627. 10.1016/j.bone.2009.10.024, 19857615.
61. Spandidos A, Wang X, Wang H, Seed B. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res 2010, 38(Database issue):D792-D799. 2808898, 19906719.
62. Etschmann B, Wilcken B, Stoevesand K, Von Der Schulenburg A, Sterner-Kock A. Selection of reference genes for quantitative real-time PCR analysis in canine mammary tumors using the GeNorm algorithm. Vet Pathol 2006, 43:934-942. 10.1354/vp.43-6-934, 17099150.