Temporal profiling and pulsed SILAC labeling identify novel secreted proteins during ex vivo osteoblast differentiation of human stromal stem cells

Molecular and Cellular Proteomics

Volumn 11, Issue 10, 2012, Pages 989-1007

  Kristensen, Lars P ^a,b   Chen, Li ^b   Nielsen, Maria Overbeck ^a,b   Qanie, Diyako W ^b   Kratchmarova, Irina ^a   Kassem, Moustapha ^b,c   Andersen, Jens S ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b ODENSE UNIVERSITY HOSPITAL   (Denmark)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; AMINO ACID; BETA 2 MICROGLOBULIN; BETA ACTIN; CATHEPSIN D; COLLAGEN TYPE 1; COMPLEMENT FACTOR H; FOLLISTATIN; FOLLISTATIN LIKE 1; GLYCOPROTEIN; HYPOCALCIN; LEGUMAIN; OSTEOCALCIN; PENTRAXIN 3; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN; PROTEIN KIAA1199; PROTEOME; SECRETOME; SELECTIN; SELECTIN LIKE OSTEOBLAST DERIVED PROTEIN; STABLE ISOTOPE; STANNIOCALCIN 2; UNCLASSIFIED DRUG;

ARTICLE; AUTOCRINE EFFECT; CELL CULTURE; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL TYPE; CONTROLLED STUDY; EX VIVO STUDY; HUMAN; HUMAN CELL; INTRACELLULAR MEMBRANE; ISOTOPE LABELING; MESENCHYMAL STEM CELL; MESENCHYMAL STROMA CELL; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; QUANTITATIVE ANALYSIS; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL STEM CELL; STABLE ISOTOPE LABELING BY AMINO ACIDS IN CELL CULTURE; STEM CELL; STROMA CELL;

AMINO ACIDS; CELL DIFFERENTIATION; CELL LINE, TRANSFORMED; CELLS, CULTURED; CHROMATOGRAPHY, LIQUID; GLYCOPROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; ISOTOPE LABELING; MESENCHYMAL STROMAL CELLS; OSTEOBLASTS; PROTEOME; PROTEOMICS; TANDEM MASS SPECTROMETRY;

EID: 84867161245     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M111.012138     Document Type: Article

References (98)

1. Fukumoto, S., and Martin, T. J. (2009) Bone as an endocrine organ. Trends Endocrinol. Metab. 20, 230-236
2. Kobayashi, Y., Udagawa, N., and Takahashi, N. (2009) Action of RANKL and OPG for osteoclastogenesis. Crit. Rev. Eukaryot. Gene Exp. 19, 61-72
3. Porter, R. L., and Calvi, L. M. (2008) Communications between bone cells and hematopoietic stem cells. Arch. Biochem. Biophys. 473, 193-200
4. Lorenzo, J., Horowitz, M., and Choi, Y. (2008) Osteoimmunology: interactions of the bone and immune system. Endocr. Rev. 29, 403-440 (Pubitemid 351831507)
5. Lee, N. K., Sowa, H., Hinoi, E., Ferron, M., Ahn, J. D., Confavreux, C., Dacquin, R., Mee, P. J., McKee, M. D., Jung, D. Y., Zhang, Z., Kim, J. K., Mauvais-Jarvis, F., Ducy, P., and Karsenty, G. (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130, 456-469 (Pubitemid 47208519)
6. Kilroy, G. E., Foster, S. J., Wu, X., Ruiz, J., Sherwood, S., Heifetz, A., Ludlow, J. W., Stricker, D. M., Potiny, S., Green, P., Halvorsen, Y. D., Cheatham, B., Storms, R. W., and Gimble, J. M. (2007) Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors. J. Cell. Physiol. 212, 702-709 (Pubitemid 47271882)
7. Haynesworth, S. E., Baber, M. A., and Caplan, A. I. (1996) Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1 alpha. J. Cell. Physiol. 166, 585-592 (Pubitemid 26095485)
8. Sze, S. K., de Kleijn, D. P., Lai, R. C., Khia Way Tan, E., Zhao, H., Yeo, K. S., Low, T. Y., Lian, Q., Lee, C. N., Mitchell, W., El Oakley, R. M., and Lim, S. K. (2007) Elucidating the secretion proteome of human embryonic stem cell-derived mesenchymal stem cells. Mol. Cell. Proteomics 6, 1680-1689 (Pubitemid 350031670)
9. Penolazzi, L., Lambertini, E., Tavanti, E., Torreggiani, E., Vesce, F., Gambari, R., and Piva, R. (2008) Evaluation of chemokine and cytokine profiles in osteoblast progenitors from umbilical cord blood stem cells by BIO-PLEX technology. Cell Biol. Int. 32, 320-325 (Pubitemid 351282502)
10. Celebi, B., Elcin, A. E., and Elcin, Y. M. (2010) Proteome analysis of rat bone marrow mesenchymal stem cell differentiation. J. Proteome Res. 9, 5217-5227
11. Kim, S., Min, W. K., Chun, S., Lee, W., Chung, H. J., Choi, S. J., Yang, S. E., Yang, Y. S., and Yoo, J. I. (2010) Protein expression profiles during osteogenic differentiation of mesenchymal stem cells derived from human umbilical cord blood. Tohoku J. Exp. Med. 221, 141-150
12. Chiellini, C., Cochet, O., Negroni, L., Samson, M., Poggi, M., Ailhaud, G., Alessi, M. C., Dani, C., and Amri, E. Z. (2008) Characterization of human mesenchymal stem cell secretome at early steps of adipocyte and osteoblast differentiation. BMC Mol. Biol. 9, 26
13. Zvonic, S., Lefevre, M., Kilroy, G., Floyd, Z. E., DeLany, J. P., Kheterpal, I., Gravois, A., Dow, R., White, A., Wu, X., and Gimble, J. M. (2007) Secretome of primary cultures of human adipose-derived stem cells: modulation of serpins by adipogenesis. Mol. Cell. Proteomics 6, 18-28 (Pubitemid 46152688)
14. Choi, Y. A., Lim, J., Kim, K. M., Acharya, B., Cho, J. Y., Bae, Y. C., Shin, H. I., Kim, S. Y., and Park, E. K. (2010) Secretome Analysis of Human BMSCs and Identification of SMOC1 as an Important ECM Protein in Osteoblast Differentiation. J. Proteome Res. 9, 2949-2956
15. Lee, M. J., Kim, J., Kim, M. Y., Bae, Y. S., Ryu, S. H., Lee, T. G., and Kim, J. H. (2010) Proteomic analysis of tumor necrosis factor-alpha-induced secretome of human adipose tissue-derived mesenchymal stem cells. J. Proteome Res. 9, 1754-1762
16. Zhu, W., Huang, L., Li, Y., Zhang, X., Gu, J., Yan, Y., Xu, X., Wang, M., Qian, H., and Xu, W. (2012) Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo. Cancer Lett. 315, 28-37
17. Lai, R. C., Chen, T. S., and Lim, S. K. (2011) Mesenchymal stem cell exosome: a novel stem cell-based therapy for cardiovascular disease. Regen. Med. 6, 481-492
18. Xiao, Z., Camalier, C. E., Nagashima, K., Chan, K. C., Lucas, D. A., de la Cruz, M. J., Gignac, M., Lockett, S., Issaq, H. J., Veenstra, T. D., Conrads, T. P., and Beck, G. R., Jr. (2007) Analysis of the extracellular matrix vesicle proteome in mineralizing osteoblasts. J. Cell. Physiol. 210, 325-335 (Pubitemid 44956877)
19. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
20. Ong, S. E., and Mann, M. (2005) Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 1, 252-262
21. Bantscheff, M., Schirle, M., Sweetman, G., Rick, J., and Kuster, B. (2007) Quantitative mass spectrometry in proteomics: a critical review. Anal. Bioanal. Chem. 389, 1017-1031 (Pubitemid 47482251)
22. Stenderup, K., Justesen, J., Clausen, C., and Kassem, M. (2003) Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33, 919-926 (Pubitemid 37543568)
23. Simonsen, J. L., Rosada, C., Serakinci, N., Justesen, J., Stenderup, K., Rattan, S. I., Jensen, T. G., and Kassem, M. (2002) Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat. Biotechnol. 20, 592-596 (Pubitemid 34595153)
24. Abdallah, B. M., Haack-Sorensen, M., Burns, J. S., Elsnab, B., Jakob, F., Hokland, P., and Kassem, M. (2005) Maintenance of differentiation potential of human bone marrow mesenchymal stem cells immortalized by human telomerase reverse transcriptase gene despite [corrected] extensive proliferation. Biochem. Biophys. Res. Commun. 326, 527-538 (Pubitemid 39642757)
25. Alvarez-Llamas, G., Szalowska, E., de Vries, M. P., Weening, D., Landman, K., Hoek, A., Wolffenbuttel, B. H., Roelofsen, H., and Vonk, R. J. (2007) Characterization of the human visceral adipose tissue secretome. Mol. Cell. Proteomics 6, 589-600 (Pubitemid 46630092)
26. Anderson, N. L., and Anderson, N. G. (2002) The human plasma proteome: history, character, and diagnostic prospects. Mol. Cell. Proteomics 1, 845-867
27. Kristensen, A. R., Schandorff, S., Høyer-Hansen, M., Nielsen, M. O., Jäättelä, M., Dengjel, J., and Andersen, J. S. (2008) Ordered organelle degradation during starvation-induced autophagy. Mol. Cell. Proteomics 7, 2419-2428
28. Yu, L., Guo, Y., Zhang, Z., Li, Y., Li, M., Li, G., Xiong, W., and Zeng, Y. (2010) SecretP: a new method for predicting mammalian secreted proteins. Peptides 31, 574-578
29. Käll, L., Krogh, A., and Sonnhammer, E. L. (2007) Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Nucleic Acids Res. 35, W429-432
30. Doherty, M. K., Hammond, D. E., Clague, M. J., Gaskell, S. J., and Beynon, R. J. (2009) Turnover of the human proteome: determination of protein intracellular stability by dynamic SILAC. J. Proteome Res. 8, 104-112
31. Lam, Y. W., Lamond, A. I., Mann, M., and Andersen, J. S. (2007) Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr. Biol. 17, 749-760 (Pubitemid 46635118)
32. Boisvert, F. M., Ahmad, Y., Gierlinski, M., Charriere, F., Lamont, D., Scott, M., Barton, G., and Lamond, A. I. (2011) A quantitative spatial proteomics analysis of proteome turnover in human cells. Mol. Cell. Proteomics.
33. Blagoev, B., and Mann, M. (2006) Quantitative proteomics to study mitogen-activated protein kinases. Methods 40, 243-250 (Pubitemid 44635297)
34. Abdallah, B. M., Haack-Sørensen, M., Fink, T., and Kassem, M. (2006) Inhibition of osteoblast differentiation but not adipocyte differentiation of mesenchymal stem cells by sera obtained from aged females. Bone 39, 181-188 (Pubitemid 43831783)
35. Zou, L., Zou, X., Chen, L., Li, H., Mygind, T., Kassem, M., and Bünger, C. (2008) Multilineage differentiation of porcine bone marrow stromal cells associated with specific gene expression pattern. J. Orthop. Res. 26, 56-64
36. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
37. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
38. Rappsilber, J., Ishihama, Y., and Mann, M. (2003) Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663-670 (Pubitemid 36176744)
39. Olsen, J. V., de Godoy, L. M., Li, G., Macek, B., Mortensen, P., Pesch, R., Makarov, A., Lange, O., Horning, S., and Mann, M. (2005) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010-2021 (Pubitemid 41830195)
40. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (Pubitemid 30007252)
41. Schandorff, S., Olsen, J. V., Bunkenborg, J., Blagoev, B., Zhang, Y., Andersen, J. S., and Mann, M. (2007) A mass spectrometry-friendly database for cSNP identification. Nat. Methods 4, 465-466 (Pubitemid 46852063)
42. Mortensen, P., Gouw, J. W., Olsen, J. V., Ong, S. E., Rigbolt, K. T., Bunkenborg, J., Cox, J., Foster, L. J., Heck, A. J., Blagoev, B., Andersen, J. S., and Mann, M. (2010) MSQuant, an open source platform for mass spectrometry-based quantitative proteomics. J. Proteome Res. 9, 393-403
43. Olsen, J. V., and Mann, M. (2004) Improved peptide identification in proteomics by two consecutive stages of mass spectrometric fragmentation. Proc. Natl. Acad. Sci. U.S.A. 101, 13417-13422 (Pubitemid 39238417)
44. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (Pubitemid 44647421)
45. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
46. Cox, J., Matic, I., Hilger, M., Nagaraj, N., Selbach, M., Olsen, J. V., and Mann, M. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 4, 698-705
47. Dennis, G., Jr., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C., and Lempicki, R. A. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, P3
48. Dopazo, J., and Carazo, J. M. (1997) Phylogenetic reconstruction using an unsupervised growing neural network that adopts the topology of a phylogenetic tree. J. Mol. Evolution 44, 226-233 (Pubitemid 27080096)
49. Herrero, J., Valencia, A., and Dopazo, J. (2001) A hierarchical unsupervised growing neural network for clustering gene expression patterns. Bioinformatics 17, 126-136 (Pubitemid 32208521)
50. Yeung, K. Y., Haynor, D. R., and Ruzzo, W. L. (2001) Validating clustering for gene expression data. Bioinformatics 17, 309-318 (Pubitemid 32421924)
51. Bendtsen, J. D., Jensen, L. J., Blom, N., Von Heijne, G., and Brunak, S. (2004) Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng. Des. Sel. 17, 349-356 (Pubitemid 39093515)
52. Hoffmann, R., and Valencia, A. (2004) A gene network for navigating the literature. Nat. Genet. 36, 664
53. Rigbolt, K. T., Vanselow, J. T., and Blagoev, B. (2011) GProX, a user-friendly platform for bioinformatics analysis and visualization of quantitative proteomics data. Mol. Cell. Proteomics 10, O110.007450
54. Kratchmarova, I., Blagoev, B., Haack-Sorensen, M., Kassem, M., and Mann, M. (2005) Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science 308, 1472-1477 (Pubitemid 40791302)
55. Palermo, C., Manduca, P., Gazzerro, E., Foppiani, L., Segat, D., and Barreca, A. (2004) Potentiating role of IGFBP-2 on IGF-II-stimulated alkaline phosphatase activity in differentiating osteoblasts. Am. J. Physiol. Endocrinol. Metab. 286, E648-657 (Pubitemid 38374964)
56. Silha, J. V., Mishra, S., Rosen, C. J., Beamer, W. G., Turner, R. T., Powell, D. R., and Murphy, L. J. (2003) Perturbations in bone formation and resorption in insulin-like growth factor binding protein-3 transgenic mice. J. Bone Miner. Res. 18, 1834-1841 (Pubitemid 37322561)
57. Kassem, M., Okazaki, R., De León, D., Harris, S. A., Robinson, J. A., Spelsberg, T. C., Conover, C. A., and Riggs, B. L. (1996) Potential mechanism of estrogen-mediated decrease in bone formation: estrogen increases production of inhibitory insulin-like growth factor-binding protein-4. Proc. Assoc. Am. Physicians 108, 155-164
58. Kiefer, M. C., Schmid, C., Waldvogel, M., Schläpfer, I., Futo, E., Masiarz, F. R., Green, K., Barr, P. J., and Zapf, J. (1992) Characterization of recombinant human insulin-like growth factor binding proteins 4, 5, and 6 produced in yeast. J. Biol. Chem. 267, 12692-12699
59. Qin, X., Wergedal, J. E., Rehage, M., Tran, K., Newton, J., Lam, P., Baylink, D. J., and Mohan, S. (2006) Pregnancy-associated plasma protein-A increases osteoblast proliferation in vitro and bone formation in vivo. Endocrinology 147, 5653-5661 (Pubitemid 44833482)
60. Kim, J. E., Kim, S. J., Lee, B. H., Park, R. W., Kim, K. S., and Kim, I. S. (2000) Identification of motifs for cell adhesion within the repeated domains of transforming growth factor-beta-induced gene, betaig-h3. J. Biol. Chem. 275, 30907-30915
61. Scott, I. C., Blitz, I. L., Pappano, W. N., Imamura, Y., Clark, T. G., Steiglitz, B. M., Thomas, C. L., Maas, S. A., Takahara, K., Cho, K. W., and Greenspan, D. S. (1999) Mammalian BMP-1/Tolloid-related metalloproteinases, including novel family member mammalian Tolloid-like 2, have differential enzymatic activities and distributions of expression relevant to patterning and skeletogenesis. Develop. Biol. 213, 283-300 (Pubitemid 29444340)
62. Safadi, F. F., Xu, J., Smock, S. L., Kanaan, R. A., Selim, A. H., Odgren, P. R., Marks, S. C., Jr., Owen, T. A., and Popoff, S. N. (2003) Expression of connective tissue growth factor in bone: its role in osteoblast proliferation and differentiation in vitro and bone formation in vivo. J. Cell. Physiol. 196, 51-62 (Pubitemid 36676442)
63. Wiktor-Jedrzejczak, W., Bartocci, A., Ferrante, A. W., Jr., Ahmed-Ansari, A., Sell, K. W., Pollard, J. W., and Stanley, E. R. (1990) Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc. Natl. Acad. Sci. U.S.A. 87, 4828-4832
64. Delany, A. M., Kalajzic, I., Bradshaw, A. D., Sage, E. H., and Canalis, E. (2003) Osteonectin-null mutation compromises osteoblast formation, maturation, and survival. Endocrinology 144, 2588-2596 (Pubitemid 36637090)
65. Hadfield, K. D., Rock, C. F., Inkson, C. A., Dallas, S. L., Sudre, L., Wallis, G. A., Boot-Handford, R. P., and Canfield, A. E. (2008) HtrA1 inhibits mineral deposition by osteoblasts: requirement for the protease and PDZ domains. J. Biol. Chem. 283, 5928-5938
66. Jellinek, D. A., Chang, A. C., Larsen, M. R., Wang, X., Robinson, P. J., and Reddel, R. R. (2000) Stanniocalcin 1 and 2 are secreted as phosphoproteins from human fibrosarcoma cells. Biochem. J. 350 Pt 2, 453-461
67. Raouf, A., Ganss, B., McMahon, C., Vary, C., Roughley, P. J., and Seth, A. (2002) Lumican is a major proteoglycan component of the bone matrix. Matrix Biol. 21, 361-367 (Pubitemid 34786472)
68. Mosig, R. A., Dowling, O., DiFeo, A., Ramirez, M. C., Parker, I. C., Abe, E., Diouri, J., Aqeel, A. A., Wylie, J. D., Oblander, S. A., Madri, J., Bianco, P., Apte, S. S., Zaidi, M., Doty, S. B., Majeska, R. J., Schaffler, M. B., and Martignetti, J. A. (2007) Loss of MMP-2 disrupts skeletal and craniofacial development and results in decreased bone mineralization, joint erosion and defects in osteoblast and osteoclast growth. Human Mol. Genetics 16, 1113-1123 (Pubitemid 47062731)
69. Tanaka, T., Ikari, K., Furushima, K., Okada, A., Tanaka, H., Furukawa, K., Yoshida, K., Ikeda, T., Ikegawa, S., Hunt, S. C., Takeda, J., Toh, S., Harata, S., Nakajima, T., and Inoue, I. (2003) Genomewide linkage and linkage disequilibrium analyses identify COL6A1, on chromosome 21, as the locus for ossification of the posterior longitudinal ligament of the spine. Am. J. Human Gen. 73, 812-822 (Pubitemid 37271885)
70. Deckers, M. M., Smits, P., Karperien, M., Ni, J., Tylzanowski, P., Feng, P., Parmelee, D., Zhang, J., Bouffard, E., Gentz, R., Löwik, C. W., and Merregaert, J. (2001) Recombinant human extracellular matrix protein 1 inhibits alkaline phosphatase activity and mineralization of mouse embryonic metatarsals in vitro. Bone 28, 14-20 (Pubitemid 32112058)
71. Barisic-Dujmovic, T., Boban, I., Adams, D. J., and Clark, S. H. (2007) Marfan-like skeletal phenotype in the tight skin (Tsk) mouse. Calcified Tissue Int. 81, 305-315 (Pubitemid 47498102)
72. Coutu, D. L., Wu, J. H., Monette, A., Rivard, G. E., Blostein, M. D., and Galipeau, J. (2008) Periostin, a member of a novel family of vitamin K-dependent proteins, is expressed by mesenchymal stromal cells. J. Biol. Chem. 283, 17991-18001
73. Gomez, D. E., Alonso, D. F., Yoshiji, H., and Thorgeirsson, U. P. (1997) Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur. J. Cell Biol. 74, 111-122 (Pubitemid 27455388)
74. Bi, Y., Stuelten, C. H., Kilts, T., Wadhwa, S., Iozzo, R. V., Robey, P. G., Chen, X. D., and Young, M. F. (2005) Extracellular matrix proteoglycans control the fate of bone marrow stromal cells. J. Biol. Chem. 280, 30481-30489 (Pubitemid 41216232)
75. Marini, J. C., Forlino, A., Cabral, W. A., Barnes, A. M., San Antonio, J. D., Milgrom, S., Hyland, J. C., Körkkö, J., Prockop, D. J., De Paepe, A., Coucke, P., Symoens, S., Glorieux, F. H., Roughley, P. J., Lund, A. M., Kuurila-Svahn, K., Hartikka, H., Cohn, D. H., Krakow, D., Mottes, M., Schwarze, U., Chen, D., Yang, K., Kuslich, C., Troendle, J., Dalgleish, R., and Byers, P. H. (2007) Consortium for osteogenesis imperfecta mutations in the helical domain of type I collagen: regions rich in lethal mutations align with collagen binding sites for integrins and proteoglycans. Human Mutation 28, 209-221
76. Mochida, Y., Duarte, W. R., Tanzawa, H., Paschalis, E. P., and Yamauchi, M. (2003) Decorin modulates matrix mineralization in vitro. Biochem. Biophys. Res. Commun. 305, 6-9 (Pubitemid 36535401)
77. Mochida, Y., Parisuthiman, D., Pornprasertsuk-Damrongsri, S., Atsawasuwan, P., Sricholpech, M., Boskey, A. L., and Yamauchi, M. (2009) Decorin modulates collagen matrix assembly and mineralization. Matrix Biol. 28, 44-52
78. Kaku, M., Mochida, Y., Atsawasuwan, P., Parisuthiman, D., and Yamauchi, M. (2007) Post-translational modifications of collagen upon BMP-induced osteoblast differentiation. Biochem. Biophys. Res. Commun. 359, 463-468 (Pubitemid 46908799)
79. Nabavi, N., Urukova, Y., Cardelli, M., Aubin, J. E., and Harrison, R. E. (2008) Lysosome dispersion in osteoblasts accommodates enhanced collagen production during differentiation. J. Biol. Chem. 283, 19678-19690
80. Billiard, J., Moran, R. A., Whitley, M. Z., Chatterjee-Kishore, M., Gillis, K., Brown, E. L., Komm, B. S., and Bodine, P. V. (2003) Transcriptional profiling of human osteoblast differentiation. J. Cell. Biochem. 89, 389-400 (Pubitemid 36547273)
81. Carano, R. A., and Filvaroff, E. H. (2003) Angiogenesis and bone repair. Drug Discovery Today 8, 980-989 (Pubitemid 37474243)
82. Gerber, H. P., and Ferrara, N. (2000) Angiogenesis and bone growth. Trends Cardiovasc. Med. 10, 223-228
83. Abe, Y., Abe, T., Aida, Y., Hara, Y., and Maeda, K. (2004) Follistatin restricts bone morphogenetic protein (BMP)-2 action on the differentiation of osteoblasts in fetal rat mandibular cells. J. Bone Miner. Res. 19, 1302-1307 (Pubitemid 41094372)
84. Aisa, M. C., Beccari, T., Costanzi, E., and Maggio, D. (2003) Cathepsin B in osteoblasts. Biochim. Biophys. Acta 1621, 149-159 (Pubitemid 36515096)
85. Morko, J., Kiviranta, R., Mulari, M. T., Ivaska, K. K., Väänänen, H. K., Vuorio, E., and Laitala-Leinonen, T. (2009) Overexpression of cathepsin K accelerates the resorption cycle and osteoblast differentiation in vitro. Bone 44, 717-728
86. Choi, S. J., Reddy, S. V., Devlin, R. D., Menaa, C., Chung, H., Boyce, B. F., and Roodman, G. D. (1999) Identification of human asparaginyl endopeptidase (legumain) as an inhibitor of osteoclast formation and bone resorption. J. Biol. Chem. 274, 27747-27753
87. Yoshiko, Y., Maeda, N., and Aubin, J. E. (2003) Stanniocalcin 1 stimulates osteoblast differentiation in rat calvaria cell cultures. Endocrinology 144, 4134-4143 (Pubitemid 37088769)
88. Ichikawa, T., Horie-Inoue, K., Ikeda, K., Blumberg, B., and Inoue, S. (2007) Vitamin K2 induces phosphorylation of protein kinase A and expression of novel target genes in osteoblastic cells. J. Mol. Endocrinol. 39, 239-247 (Pubitemid 350047645)
89. Gilges, D., Vinit, M. A., Callebaut, I., Coulombel, L., Cacheux, V., Romeo, P. H., and Vigon, I. (2000) Polydom: a secreted protein with pentraxin, complement control protein, epidermal growth factor and von Willebrand factor A domains. Biochem. J. 352 Pt 1, 49-59
90. Shur, I., Socher, R., Hameiri, M., Fried, A., and Benayahu, D. (2006) Molecular and cellular characterization of SEL-OB/SVEP1 in osteogenic cells in vivo and in vitro. J. Cell. Physiol. 206, 420-427 (Pubitemid 43062811)
91. Shur, I., Zemer-Tov, E., Socher, R., and Benayahu, D. (2007) SVEP1 expression is regulated in estrogen-dependent manner. J. Cell. Physiol. 210, 732-739 (Pubitemid 46185042)
92. Lee, G. W., Lee, T. H., and Vilcek, J. (1993) TSG-14, a tumor necrosis factor- and IL-1-inducible protein, is a novel member of the pentaxin family of acute phase proteins. J. Immunol. 150, 1804-1812 (Pubitemid 23129656)
93. Fedarko, N. S., Fohr, B., Robey, P. G., Young, M. F., and Fisher, L. W. (2000) Factor H binding to bone sialoprotein and osteopontin enables tumor cell evasion of complement-mediated attack. J. Biol. Chem. 275, 16666-16672 (Pubitemid 30398895)
94. Estrada, R., Li, N., Sarojini, H., An, J., Lee, M. J., and Wang, E. (2009) Secretome from mesenchymal stem cells induces angiogenesis via Cyr61. J. Cell. Physiol. 219, 563-571
95. Molina, H., Yang, Y., Ruch, T., Kim, J. W., Mortensen, P., Otto, T., Nalli, A., Tang, Q. Q., Lane, M. D., Chaerkady, R., and Pandey, A. (2009) Temporal profiling of the adipocyte proteome during differentiation using a fiveplex SILAC based strategy. J. Proteome Res. 8, 48-58
96. Roelofsen, H., Dijkstra, M., Weening, D., de Vries, M. P., Hoek, A., and Vonk, R. J. (2009) Comparison of isotope-labeled amino acid incorporation rates (CILAIR) provides a quantitative method to study tissue secretomes. Mol. Cell. Proteomics 8, 316-324
97. Yeung, B. H., Law, A. Y., and Wong, C. K. (2012) Evolution and roles of stanniocalcin. Mol. Cell. Endocrinol. 349, 272-280
98. Takei, Y., Yamamoto, H., Sato, T., Otani, A., Kozai, M., Masuda, M., Taketani, Y., Muto-Sato, K., Lanske, B., and Takeda, E. (2012) Stanniocalcin 2 is associated with ectopic calcification in alpha-klotho mutant mice and inhibits hyperphosphatemia-induced calcification in aortic vascular smooth muscle cells. Bone 50, 998-1005