Proteomic characterization of biogenesis and functions of matrix vesicles released from mineralizing human osteoblast-like cells

Journal of Proteomics

Volumn 74, Issue 7, 2011, Pages 1123-1134

  Thouverey, Cyril ^a,b,c,d,e,f   Malinowska, Agata ^g   Balcerzak, Marcin ^a   Strzelecka Kiliszek, Agnieszka ^a   Buchet, René ^b,c,d,e,f   Dadlez, Michal ^g,h   Pikula, Slawomir ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITÉ LYON 1   (France)

^d UNIVERSITÉ DE LYON   (France)

^e CPE LYON   (France)

^f UNIVERSITÉ LYON 1   (France)

^g INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^h UNIVERSITY OF WARSAW   (Poland)

Author keywords

Apical microvilli; LC ESI MS MS; Matrix vesicles; Mineralization; Osteoblasts

Indexed keywords

ACTIN; BICARBONATE SODIUM COTRANSPORTER; COFILIN 1; GELSOLIN; INORGANIC PYROPHOSPHATASE; MYOSIN; PROTEOME; RAB PROTEIN; SPHINGOMYELIN PHOSPHODIESTERASE;

ARTICLE; BIOGENESIS; CELL FUNCTION; CONTROLLED STUDY; CYTOPLASM VESICLE; ELECTROSPRAY MASS SPECTROMETRY; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; MICROVILLUS; MINERALIZATION; OSTEOBLAST; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS;

BONE MATRIX; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; CYTOPLASMIC VESICLES; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; HUMANS; MICROVILLI; OSTEOBLASTS; OSTEOGENESIS; PROTEOME; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TUMOR CELLS, CULTURED;

EID: 79957656624     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.04.005     Document Type: Article

References (71)

1. Anderson H.C. Electron microscopic studies of induced cartilage development and calcification. J Cell Biol 1967, 35:81-101.
2. Anderson H.C., Reynolds J.J. Pyrophosphate stimulation of calcium uptake into cultured embryonic bones. Fine structure of matrix vesicles and their role in calcification. Dev Biol 1973, 34:211-227.
3. Anderson H.C. Molecular biology of matrix vesicles. Clin Orthop Relat Res 1995, 314:266-280.
4. Wuthier R.E., Majeska R.J., Collins G.M. Biosynthesis of matrix vesicles in epiphyseal cartilage. I. In vivo incorporation of 32P orthophosphate into phospholipids of chondrocyte, membrane, and matrix vesicle fractions. Calcif Tissue Res 1977, 23:135-139.
5. Brighton C.T., Hunt R.M. Histochemical localization of calcium in growth plate mitochondria and matrix vesicles. Fed Proc 1976, 35:143-147.
6. Wu L.N., Ishikawa Y., Sauer G.R., Genge B.R., Mwale F., Mishima H., Wuthier R.E. Morphological and biochemical characterization of mineralizing primary cultures of avian growth plate chondrocytes: evidence for cellular processing of Ca2+ and Pi prior to matrix mineralization. J Cell Biochem 1995, 57:218-237.
7. Hale J.E., Wuthier R.E. The mechanism of matrix vesicle formation. Studies on the composition of chondrocyte microvilli and on the effects of microfilament-perturbing agents on cellular vesiculation. J Biol Chem 1987, 262:1916-1925.
8. Thouverey C., Strzelecka-Kiliszek A., Balcerzak M., Buchet R., Pikula S. Matrix vesicles originate from apical membrane microvilli of mineralizing osteoblast-like Saos-2 cells. J Cell Biochem 2009, 106:127-138.
9. Wuthier R.E. Effect of phospholipids on the transformation of amorphous calcium phosphate to hydroxapatite in vitro. Calcif Tissue Res 1975, 19:197-210.
10. 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., Beck G.R.Jr. Analysis of the extracellular matrix vesicle proteome in mineralizing osteoblasts. J Cell Physiol 2007, 210:325-335.
11. Balcerzak M., Malinowska A., Thouverey C., Sekrecka A., Dadlez M., Buchet R., Pikula S. Proteome analysis of matrix vesicles isolated from femurs of chicken embryo. Proteomics 2008, 8:192-205.
12. Rosenthal A.K., Gohr C.M., Ninomiya J., Wakim B.T. Proteomic analysis of articular cartilage vesicles from normal and osteoarthritic cartilage. Arthritis Rheum 2011, 63:401-411.
13. Xiao Z., Blonder J., Zhou M., Veensta T.D. Proteomic analysis of extracellular matrix and vesicles. J Proteomics 2009, 72:34-45.
14. Golub E.E. Role of matrix vesicles in biomineralization. Biochim Biophys Acta 2009, 1790:1592-1598.
15. Register T.C., McLean F.M., Low M.G., Wuthier R.E. Roles of alkaline phosphatase and labile internal mineral in matrix vesicle-mediated calcification. J Biol Chem 1986, 261:9354-9360.
16. Johnson K., Moffa A., Chen Y., Pritzker K., Goding J., Terkeltaub R. Matrix vesicle plasma cell membrane glycoprotein-1 regulates mineralization by murine osteoblastic MC3T3 cells. J Bone Miner Res 1999, 14:883-892.
17. Zaka R., Williams C.J. The inorganic phosphate/inorganic pyrophosphate axis in the mineralization of cartilage and bone. Curr Opin Orthop 2007, 18:454-459.
18. Thouverey C., Bechkoff G., Pikula S., Buchet R. Inorganic pyrophosphate as a regulator of hydroxyapatite or calcium pyrophosphate dihydrate mineral deposition by matrix vesicles. Osteoarthritis Cartilage 2009, 17:64-72.
19. Hessle L., Johnson K.A., Anderson H.C., Narisawa S., Sali A., Goding J.W., Terkeltaub R., Millan J.L. Tissue-nonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization. Proc Natl Acad Sci USA 2002, 99:9445-9449.
20. Einhorn T.A., Gordon S.L., Siegel S.A., Hummel C.F., Avitable M.J., Carty R.P. Matrix vesicle enzymes in human osteoarthritis. J Orthop Res 1985, 3:160-169.
21. Stewart A.J., Roberts S.J., Seawright E., Davey M.G., Fleming R.H., Farquharson C. The presence of PHOSPHO1 in matrix vesicles and its developmental expression prior to skeletal mineralization. Bone 2006, 39:1000-1007.
22. Montessuit C., Caverzasio J., Bonjour J.P. Characterization of a Pi transport system in cartilage matrix vesicles. Potential role in the calcification process. J Biol Chem 1991, 266:17791-17797.
23. Wu L.N., Sauer G.R., Genge B.R., Valhmu W.B., Wuthier R.E. Effects of analogues of inorganic phosphate and sodium ion on mineralization of matrix vesicles isolated from growth plate cartilage of normal rapidly growing chickens. J Inorg Biochem 2003, 94:221-235.
24. Kirsch T., Nah H.D., Demuth D.R., Harrison G., Golub E.E., Adams S.L., Pacifici M. Annexin V-mediated calcium flux across membranes is dependent on the lipid composition: implications for cartilage mineralization. Biochemistry 1997, 36:3359.
25. Kirsch T., Harisson G., Golub E.E., Nah H.D. The roles of annexins and types II and X collagen in matrix vesicle-mediated mineralization of growth plate cartilage. J Biol Chem 2000, 275:35577-35583.
26. Peress N.S., Anderson H.C., Sajdera S.W. The lipids of matrix vesicles from bovine fetal epiphyseal cartilage. Calcif Tissue Res 1974, 14:275-281.
27. Wuthier R.E. Lipid composition of isolated epiphyseal cartilage cells, membranes and matrix vesicles. Biochim Biophys Acta 1975, 409:128-143.
28. Wu L.N., Yoshimori T., Genge B.G., Sauer G.R., Kirsch T., Ishikawa Y., Wuthier R.E. Characterization of the nucleational core complex responsible for mineral induction by growth plate cartilage matrix vesicles. J Biol Chem 1993, 268:25084-25094.
29. Sauer G.R., Genge B.R., Wu L.N., Donachy J.E. A facilitative role for carbonic anhydrase activity in matrix vesicle mineralization. Bone Miner 1994, 26:69-79.
30. Wu L.N., Genge B.R., Kang M.W., Arsenault A.L., Wuthier R.E. Changes in phospholipid extractability and composition accompany mineralization of chicken growth plate cartilage matrix vesicles. J Biol Chem 2002, 277:5126-5133.
31. Balcerzak M., Pikula S., Buchet R. Phosphorylation-dependent phospholipase D activity of matrix vesicles. FEBS Lett 2006, 580:5676-5680.
32. Wu L.N., Genge B.R., Wuthier R.E. Association between proteoglycans and matrix vesicles in the extracellular matrix of growth plate cartilage. J Biol Chem 1991, 266:1187-1194.
33. Dean D.D., Schwartz Z., Bonewald L., Muniz O.E., Morales S., Gomez R., Brooks B.P., Qiao M., Howell D.S., Boyan B.D. Matrix vesicles produced by osteoblast-like cells in culture become significantly enriched in proteoglycan-degrading metalloproteinases after addition of beta-glycerophosphate and ascorbic acid. Calcif Tissue Int 1994, 54:399-408.
34. D'Angelo M., Billings P.C., Pacifici M., Leboy P.S., Kirsch T. Authentic matrix vesicles contain active metalloproteases (MMP). A role for matrix vesicle-associated MMP-13 in activation of transforming growth factor-beta. J Biol Chem 2001, 276:11347-11353.
35. Shevchenko A., Wilm M., Vorm O., Jensen O.N., Podtelejnikov A.V., Neubauer G., Shevchenko A., Mortensen P., Mann M. A strategy for identifying gel-separated proteins in sequence databases by MS alone. Biochem Soc Trans 1996, 24:893-896.
36. Hausser H.J., Brenner R.E. Low doses and high doses of heparin have different effects on osteoblast-like Saos-2 cells in vitro. J Cell Biochem 2004, 91:1062-1073.
37. Gillette J.M., Nielsen-Preiss S.M. The role of annexin 2 in osteoblastic mineralization. J Cell Sci 2004, 117:441-449.
38. Bonilha V.L., Bhattacharya S.K., West K.A., Sun J., Crabb J.W., Rayborn M.E., Hollyfield J.G. Proteomic characterization of isolated retinal pigment epithelium microvilli. Mol Cell Proteomics 2004, 3:1119-1127.
39. Cutillas P.R., Biber J., Marks J., Jacob R., Stieger B., Cramer R., Waterfield M., Burlingame A.L., Unwin R.J. Proteomic analysis of plasma membrane vesicles isolated from the rat renal cortex. Proteomics 2005, 5:101-112.
40. Paradela A., Bravo S.B., Henríquez M., Riquelme G., Gavilanes F., González-Ros J.M., Albar J.P. Proteomic analysis of apical microvillous membranes of syncytiotrophoblast cells reveals a high degree of similarity with lipid rafts. J Proteome Res 2005, 4:2435-2441.
41. Donowitz M., Singh S., Salahuddin F.F., Hogema B.M., Chen Y., Gucek M., Cole R.N., Ham A., Zachos N.C., Kovbasnjuk O., Lapierre L.A., Broere N., Goldenring J., Li X. Proteome of murine jejunal brush border membrane vesicles. J Proteome Res 2007, 6:4068-4079.
42. Sawada N., Taketani Y., Amizuka N., Ichikawa M., Ogawa C., Nomoto K., Nashiki K., Sato T., Arai H., Isshiki M., Segawa H., Yamamoto H., Miyamoto K., Takeda E. Caveolin-1 in extracellular matrix vesicles secreted from osteoblasts. Bone 2007, 41:52-58.
43. Hosokawa R., Uchida Y., Fujiwara S., Noguchi T. Lactate dehydrogenase isoenzymes are present in matrix vesicles. J Biol Chem 1988, 263:10045-10047.
44. Fedde K.N. Human osteosarcoma cells spontaneously release matrix-vesicle-like structures with the capacity to mineralize. Bone Miner 1992, 17:145-151.
45. Lucero H.A., Robbins P.W. Lipid rafts-protein association and the regulation of protein activity. Arch Biochem Biophys 2004, 426:208-224.
46. Foster L.J., De Hoog C.L., Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci USA 2003, 100:5813-5818.
47. Kitt K.N., Hernández-Deviez D., Ballantyne S.D., Spiliotis E.T., Casanova J.E., Wilson J.M. Rab14 regulates apical targeting in polarized epithelial cells. Traffic 2008, 9:1218-1231.
48. Simpson J.C., Griffiths G., Wessling-Resnick M., Fransen J.A., Bennett H., Jones A.T. A role for the small GTPase Rab21 in the early endocytic pathway. J Cell Sci 2004, 117:6297-6311.
49. Vonderheit A., Helenius A. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol 2005, 3:e233.
50. Williams D., Pessin J.E. Mapping of R-SNARE function at distinct intracellular GLUT4 trafficking steps in adipocytes. J Cell Biol 2008, 180:375-387.
51. Low S.H., Chapin S.J., Wimmer C., Whiteheart S.W., Kömüves L.G., Mostov K.E., Weimbs T. The SNARE machinery is involved in apical plasma membrane trafficking in MDCK cells. J Cell Biol 1998, 141:1503-1513.
52. St Johnston D. The intracellular localization of messenger mRNAs. Cell 1995, 81:161-170.
53. Mili S., Moissoglu K., Macara I.G. Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature 2008, 453:115-119.
54. Mitton E., Gohr C.M., McNally M.T., Rosenthal A.K. Articular cartilage vesicles contain RNA. Biochem Biophys Res Commun 2009, 388:533-538.
55. Borg T.K., Runyan R.B., Wuthier R.E. Correlation of freeze-fracture and scanning electron microscopy of epiphyseal chondrocytes. Calcif Tissue Res 1978, 26:237-241.
56. Mooseker M.S., Tilney L.G. Organization of an actin filament-membrane complex. Filament polarity and membrane attachment in the microvilli of intestinal epithelial cells. J Cell Biol 1975, 67:725-743.
57. Fath K.R., Burgess D.R. Microvillus assembly. Not actin alone. Curr Biol 1995, 5:591-593.
58. Aspenström P., Fransson A., Saras J. Rho GTPases have diverse effects on the organization of the actin filament system. Biochem J 2004, 377:327-337.
59. Booth A.G., Kenny J. A morphometric and biochemical investigation of the vesiculation of kidney microvilli. J Cell Sci 1976, 21:449-463.
60. Hearn P.R., Russel R.G.G., Farmer J. The formation and orientation of brush border vesicles from rat duodenal mucosa. J Cell Sci 1981, 47:227-236.
61. Pope B.J., Zierler-Gould K.M., Kühne R., Weeds A.G., Ball L.J. Solution structure of human cofilin: actin binding, pH sensitivity, and relationship to actin-depolymerizing factor. J Biol Chem 2004, 279:4840-4848.
62. Janmey P.A., Chaponnier C., Lind S.E., Zaner K.S., Stossel T.P., Yin H.L. Interactions of gelsolin and gelsolin-actin complexes with actin. Effects of calcium on actin nucleation, filament severing, and end blocking. Biochemistry 1985, 24:3714-3723.
63. Larsson C. Protein kinase C and the regulation of the actin cytoskeleton. Cell Signal 2006, 18:276-284.
64. Burgess D.R., Prum B.E. Reevaluation of brush border motility: calcium induces core filament solution and microvillar vesiculation. J Cell Biol 1982, 94:97-107.
65. McConnel R.E., Tyska M.J. Myosin-1a powers the sliding of apical membrane along microvillar actin bundles. J Cell Biol 2007, 177:671-681.
66. Mooseker M.S. Brush border motility. Microvillar contraction in Triton-treated brush borders isolated from intestinal epithefium. J Cell Biol 1976, 71:417-432.
67. Levade T., Jaffrézou J.P. Signalling sphingomyelinases: which, where, how and why?. Biochim Biophys Acta 1999, 1438:1-17.
68. Aubin I., Adams C.P., Opsahl S., Septier D., Bishop C.E., Auge N., Salvayre R., Negre-Salvayre A., Goldberg M., Guénet J.L., Poirier C. A deletion in the gene encoding sphingomyelin phosphodiesterase 3 (Smpd3) results in osteogenesis and dentinogenesis imperfecta in the mouse. Nat Genet 2005, 37:803-805.
69. Yadav M.C., Simão A.M., Narisawa S., Huesa C., McKee M.D., Farquharson C., Millán J.L. Loss of skeletal mineralization by the simultaneous ablation of PHOSPHO1 and alkaline phosphatase function: a unified model of the mechanisms of initiation of skeletal calcification. J Bone Miner Res 2011, 26:286-297.
70. Salzer U., Hinterdorfer P., Hunger U., Borken C., Prohaska R. Ca2+-dependent vesicle release from erythrocytes involves stomatin-specific lipid rafts, synexin (annexin VII), and sorcin. Blood 2002, 99:2569-2577.
71. Randall J., Thorne T., Delpire E. Partial cloning and characterization of Slc12a2: the gene encoding the secretory Na+-K+-2Cl? cotransporter. Am J Physiol 1997, 273:C1267-C1277.