Plasma membrane factor XIIIA transglutaminase activity regulates osteoblast matrix secretion and deposition by affecting microtubule dynamics

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Al Jallad, Hadil F ^a   Myneni, Vamsee D ^a   Piercy Kotb, Sarah A ^a,c   Chabot, Nicolas ^b   Mulani, Amina ^b   Keillor, Jeffrey W ^b   Kaartinen, Mari T ^a,c  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 13A; COLLAGEN TYPE 1; DANSYL CHLORIDE; FIBRONECTIN; GLUTAMIC ACID; TUBULIN; BLOOD CLOTTING FACTOR 13; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2;

ARTICLE; CELL DIFFERENTIATION; CELL MEMBRANE; CELL METABOLISM; CELL SECRETION; CELL SURFACE; CELL TRACKING; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; EXTRACELLULAR MATRIX; IMMUNOFLUORESCENCE MICROSCOPY; MICROTUBULE; MOLECULAR DYNAMICS; MOLECULAR PROBE; MOLECULAR WEIGHT; OSTEOBLAST; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN SYNTHESIS REGULATION; PROTEIN TARGETING; REGULATORY MECHANISM; WESTERN BLOTTING; ANIMAL; BONE DEVELOPMENT; CELL STRAIN 3T3; CYTOLOGY; ENZYMOLOGY; METABOLISM; MOUSE; PHYSIOLOGY; SECRETION;

3T3 CELLS; ANIMALS; CELL DIFFERENTIATION; CELL MEMBRANE; EXTRACELLULAR MATRIX; FACTOR XIII; FACTOR XIIIA; GTP-BINDING PROTEINS; MICE; MICROTUBULES; OSTEOBLASTS; OSTEOGENESIS; TRANSGLUTAMINASES;

EID: 79251631214     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015893     Document Type: Article

References (101)

1. Sommerfeldt DW, Rubin CT (2001) Biology of bone and how it orchestrates the form and function of skeleton. Eur Spine J 10: S86-S95.
2. Raggatt LJ, Partridge NC (2010) Cellular and molecular mechanisms of bone remodelling. J Biol Chem 285: 25103-25108.
3. Franceschi RT, Xiao G, Jiang D, Gopalakrishnan R, Yang S, et al. (2003) Multiple signaling pathways converge on the Cbfa1/Runx2 transcription factor to regulate osteoblast differentiation. Connect Tiss Res 44: S1,109-16.
4. Komori T (2006) Regulation of osteoblast differentiation by transcription factors. J Cell Biochem 99: 1233-9.
5. Huang W, Yang S, Shao J, Li YP (2007) Signaling and transcriptional regulation in osteoblast commitment and differentiation. Front Biosci 12: 3068-92.
6. McKee MD, Addison W, Kaartinen MT (2006) Hierarchies of extracellular matrix and mineral organization in bone of the craniofacial complex and skeleton. Cells Tissues Organs 181: 176-88.
7. Franceschi RT, Young J (1990) Regulation of alkaline phosphatase by 1,25- dihydroxyvitamin D3 and ascorbic acid in bone-derived cells. J Bone Miner Res 5: 1157-67.
8. Franceschi RT, Iyer BS (1992) Relationship between collagen synthesis and expression of the osteoblast phenotype in MC3T3-E1 cells. J Bone Miner Res 2: 235-46.
9. Franceschi RT, Iyer BS, Cui Y (1994) Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3-E1 cells. J Bone Miner Res 9: 843-54.
10. Murshed M, Harmey D, Millán JL, McKee MD, Karsenty G (2005) Unique coexpression in osteoblasts of broadly expressed genes accounts for the spatial restriction of ECM mineralization to bone. Genes Dev 19: 1093-104.
11. Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20: 33-43.
12. Canty EG, Kadler KE (2005) Procollagen trafficking, processing and fibrillogenesis. J Cell Sci Apr 1;118(Pt 7): 1341-53.
13. Nabavi N, Urukova Y, Cardelli M, Aubin JE, Harrison RE (2008) Lysosome dispersion in osteoblasts accommodates enhanced collagen production during differentiation. J Biol Chem 283: 19678-90.
14. McDonald JA, Kelley DG, Broekelmann TJ (1982) Role of fibronectin in collagen deposition; Fab' to the gelatin-binding domain of fibronectin inhibits both fibronectin and collagen organization in fibroblast extracellular matrix. J Cell Biol 92: 485-492.
15. Speranza ML, Valentini G, Calligaro A (1987) Influence of fibronectin on the fibrillogenesis of type I and type III collagen. Coll Relat Res 2: 115-123.
16. Al-Jallad HF, Nakano Y, Chen JLY, McMillan E, Lefebvre C, et al. (2006) Transglutaminase activity regulates osteoblast differentiation and matrix mineralization in MC3T3-E1 osteoblast cells. Matrix Biol 25: 135-148.
17. Aeschlimann D, Thomazy W (2000) Protein crosslinking in assembly and remodelling of extracellular matrices: the role of transglutaminases. Connect Tissue Res 41: 1-27.
18. Griffin M, Casadio R, Bergamini CM (2002) Transglutaminases: nature's biological glues. Biochem J 368: 377-96.
19. Lorand L, Graham RM (2003) Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 4: 140-56.
20. Iismaa SE, Mearns BM, Lorand L, Graham RM (2009) Transglutaminases and disease: lessons from genetically engineered mouse models and inherited disorders. Physiol Rev 89: 991-1023.
21. Aeschlimann D, Paulsson MJ (1991) Cross-linking of laminin-nidogen complexes by tissue transglutaminase. A novel mechanism for basement membrane stabilization. J Biol Chem 266: 15308-17.
22. Achyuthan KE, Rowland TC, Birckbichler PJ, Lee KN, Bishop PD, et al. (1996) Hierarchies in the binding of human factor XIII, factor XIIIa, and endothelial cell transglutaminase to human plasma fibrinogen, fibrin, and fibronectin. Mol Cell Biochem 162: 43-9.
23. Lynch GW, Slayter HS, Miller BE, McDonagh J (1987) Characterization of thrombospondin as a substrate for Factor XIII. J Biol Chem 262: 1772-1778.
24. Prince CW, Dickie D, Krumdieck CL (1991) Osteopontin, a substrate for transglutaminase and factor XIII activity. Biochem Biophys Res Commun 177: 1205-1210.
25. Sørensen ES, Rasmussen LK, Møller L, Jensen PH, Hørup P, et al. (1994) Localization of transglutaminase-reactive glutamine residues in bovine osteopontin. J Biochem 304: 13-16.
26. Kaartinen MT, Pirhonen A, Linnala-Kankkunen A, Mäenpää PH (1997) Transglutaminase-catalyzed crosslinking of osteopontin is inhibited by osteocalcin. J Biol Chem 27: 22736-22741.
27. Esposito C, Caputo I (2005) Mammalian transglutaminases. Identification of substrates as a key to physiological function and physiopathological relevance. FEBS J 272: 615-631.
28. Facchiano F, Facchiano A, Facchiano AM (2006) The role of transglutaminase-2 and its substrates in human diseases. Front Biosci 11: 1758-73.
29. Kaartinen MT, El-Maadawy S, Räsänen NH, McKee MD (2002) Transglutaminase and its substrates in bone. J Bone Miner Res 12: 2161-2173.
30. Nakano Y, Al-Jallad HF, Mousa A, Kaartinen MT (2007) Expression and localization of plasma transglutaminase factor XIIIA in bone. J Histochem Cytochem 55: 675-85.
31. Aeschlimann D, Wetterwald A, Fleish H, Paulsson M (1993) Expression of tissue transglutaminase in skeletal tissue correlates with events of terminal differentiation of chondrocytes. J Cell Biol 120: 1461-1470.
32. Aeschlimann D, Mosher D, Paulsson M (1996) Tissue transglutaminase and factor XIII in cartilage and bone remodeling. Semin Thromb Hemost 22: 437-443.
33. Gentile V, Thomazy V, Piacentini M, Fesus L, Davies PJ (1992) Expression of tissue transglutaminase in Balb-C 3T3 fibroblasts: effects on cellular morphology and adhesion. J Cell Biol 119: 463-474.
34. Jones RA, Nicholas B, Mian S, Davies PJ, Griffin M (1997) Reduced expression of tissue transglutaminase in a human endothelial cell line leads to changes in cell spreading, cell adhesion and reduced polymerization of fibronectin. J Cell Sci 110: 2461-2472.
35. Verderio E, Nicholas B, Gross S, Griffin M (1998) Regulated expression of tissue transglutaminase in swiss 3T3 fibroblasts: effects on the processing of fibronectin, cell attachment, and cell death. Exp Cell Res 239: 119-138.
36. Gaudry CA, Vederio E, Aeschlimann D, Cox A, Smith C, et al. (1999) Cell surface localization of tissue transglutaminase independent on a fibronectinbinding site in its N-terminal ß-sandwich domain. J Biol Chem 274: 30707-30714.
37. Akimov SS, Krylov D, Fleischman LF, Belkin AM (2000) Tissue transglutaminase is an integrin-binding adhesion coreceptor for fibronectin. J Cell Biol 148: 825-838.
38. Akimov SS, Belkin AM (2001) Cell-surface transglutaminase promotes fibronectin assembly via interaction with the gelatin-binding domain of fibronectin: a role in TGFb-dependent matrix deposition. J Cell Sci 114: 2989-3000.
39. Forsprecher J, Wang Z, Nelea V, Kaartinen MT (2009) Enhanced osteoblast adhesion on transglutaminase 2-crosslinked fibronectin. Amino Acids 36: 747-53.
40. Collighan RJ, Griffin M (2009) Transglutaminase 2 cross-linking of matrix proteins: biological significance and medical applications. Amino Acids 36: 659-70.
41. Janiak A, Zemskov EA, Belkin AM (2006) Cell surface transglutaminase promotes RhoA activation via integrin clustering and suppression of the Srcp190PhoGAP signaling pathway. Mol Biol Cell 17: 1606-1619.
42. Nurminskaya M, Magee C, Faverman L, Linsenmayer TF (2003) Chondrocyte- derived transglutaminase promotes maturation of preosteoblasts in periosteal bone. Dev Biol 263: 139-152.
43. Faverman L, Mikhaylova L, Malmquist J, Nurminskaya M (2008) Extracellular transglutaminase 2 activates [beta]-catenin signaling in calcifying vascular smooth muscle cells. FEBS Lett 582: 1552-1557.
44. Nurminskaya M, Magee C, Nurminsky D, Linsenmayer TF (1998) Plasma transglutaminase in hyperthophic chondrocytes: expression and cell-specific intracellular activation produce cell death and externalization. J Cell Biol 142: 1135-1144.
45. Nurminskaya MV, Linsenmayer TF (2002) Immunological analysis of transglutaminase factor XIIIA expression in mouse embryonic growth plate. J Orthop Res 20: 575-578.
46. Nurminskaya MV, Recheis B, Nimpf J, Magee C, Linsenmayer TF (2002) Transglutaminase Factor XIIIA in cartilage of developing avian long bones. Dev Dyn 223: 24-32.
47. Johnson KA, van Etten D, Nanda N, Graham RM, Terkeltaub RA (2003) Distinct transglutaminase 2-independent and transglutaminase 2-dependent pathways mediate articular chondrocyte hypertrophy. J Biol Chem 278: 18824-18832.
48. Johnson KA, Terkeltaub RA (2005) External GTP-bound transglutaminase 2 is a molecular switch for chondrocyte hypertrophic differentiation and calcification. J Biol Chem 280: 15004-15012.
49. Johnson KA, Rose DM, Terkeltaub RA (2008) Factor XIIIA mobilizes transglutaminase 2 to induce chondrocyte hypertrophic differentiation. J Cell Sci 121: 2256-2264.
50. Muszbek L, Yee VC, Hevessy Z (1999) Blood coagulation factor XIII: structure and function. Thromb Res 94: 271-305.
51. Lorand L (2005) Factor XIII and the clotting of fibrinogen: from basic research to medicine. J Thromb Haemost 3: 1337-48.
52. Nurminskaya M, Kaartinen MT (2006) Transglutaminases in mineralized tissues. Front Biosci 11: 1591-606.
53. De Laurenzi V, Melino G (2001) Gene disruption of tissue transglutaminase. Mol. Cell Biol 21: 148-55.
54. Nanda N, Iismaa SE, Owens WA, Husain A, Mackay F, et al. (2001) Targeted inactivation of Gh/tissue transglutaminase II. J Biol Chem 276: 20673-20678.
55. Lauer P, Matzner HJ, Zettlmeissl G, Li M, Smith AG, et al. (2002) Targeted inactivation of the mouse locus encoding coagulation factor XIII-A: hemostatic abnormalities in mutant mice and characterization of the coagulation deficit. Thromb Haemost 88: 967-74.
56. Tarantino U, Oliva F, Taurisano G, Orlandi A, Pietroni V, et al. (2009) FXIIIA and TGF-beta over-expression produces normal musculo-skeletal phenotype in TG2-/- mice. Amino Acids 36: 679-84.
57. Cordell PA, Kile BT, Standeven KF, Josefsson EC, Pease RJ, et al. (2010) Association of coagulation factor XIII-A with Golgi proteins within monocytemacrophages: implications for subcellular trafficking and secretion. Blood 115: 2674-81.
58. Zemskov EA, Mikhailenko I, Strickland DK, Belkin AM (2007) Cell-surface transglutaminase undergoes internalization and lysosomal degradation: an essential role for LRP1. J Cell Sci 120: 3188-99.
59. Xiao G, Gopalakrishnan R, Jiang D, Reith E, Benson MD, et al. (2002) Bone morphogenetic proteins, extracellular matrix, and mitogen-activated protein kinase signaling pathways are required for osteoblast-specific gene expression and differentiation in MC3T3-E1 cells. J Bone Miner Res 17: 101-10.
60. Keillor JW, Chica RA, Chabot N, Vinci V, Pardin C, et al. (2008) The bioorganic chemistry of transglutaminase: From mechanism to inhibition and engineering. Can J Chem 86: 271-276.
61. Folk JE (1983) Mechanism and basis for specificity of transglutaminasecatalyzed epsilon-(gamma-glutamyl) lysine bond formation. Adv Enzymol Relat Areas Mol Biol 54: 1-56.
62. de Macédo P, Marrano C, Keillor JW (2002) Synthesis of dipeptide-bound epoxides and alpha,beta-unsaturated amides as potential irreversible transglutaminase inhibitors. Bioorg Med Chem 10: 355-60.
63. Bernstein EF, Chen YQ, Kopp JB, Fisher L, Brown DB, et al. (1996) Longterm sun exposure alters the collagen of the papillary dermis. Comparison of sun-protected and photoaged skin by northern analysis, immunohistochemical staining, and confocal laser scanning microscopy. J Am Acad Dermatol 34: 209-18.
64. Dzamba BJ, Wu H, Jaenisch R, Peters DM (1993) Fibronectin binding site in type I collagen regulates fibronectin fibril formation. J Cell Biol 121: 1165-1172.
65. Schmid I, Uittenbogaart CH, Giorgi JV (1991) A gentle fixation and permeabilization method for combined cell surface and intracellular staining with improved precision in DNA quantification. Cytometry 12: 279-85.
66. Allan VJ (2000) Protein localization by fluorescence microscopy: A Practical Approach. In: Hames BD, ed. The Practical Approach Series, New York: Oxford University Press Inc. pp 4-20.
67. Pinkas DM, Strop P, Brunger AT, Khosla C (2007) Transglutaminase 2 undergoes a large conformational change upon activation. PLoS Biol 5: e327.
68. Schmoranzer J, Simon SM (2003) Role of microtubules in fusion of Post-Golgi vesicles to the plasma membrane. Mol Biol Cell 14: 1558-1569.
69. Verhage M, Toonen RF (2007) Regulated exocytosis: merging ideas on fusing membranes, Curr Opin Cell Biol 19: 402-408.
70. Diegelmann RF, Peterkofsky B (1972) Inhibition of collagen secretion from bone and cultured fibroblasts by microtubular disruptive drugs. Proc Natl Acad Sci U S A 69: 892-6.
71. Zhang Q, Magnusson MK, Mosher DF (1997) Lysophosphatidic acid and microtubule-destabilizing agents stimulate fibronectin matrix assembly through Rho-dependent actin stress fiber formation and cell contraction. Mol Biol Cell 8: 1415-25.
72. Smyth JW, Hong TT, Gao D, Vogan JM, Jensen BC, et al. (2010) Limited forward trafficking of connexin 43 reduces cell-cell coupling in stressed human and mouse myocardium. J Clin Invest 120: 266-79.
73. Palazzo AF, Eng CH, Schlaepfer DD, Marcantonio EE, Gundersen GG (2004) Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 303: 836-839.
74. Zhao H, Ito Y, Chappel J, Andrews NW, Teitelbaum SL, et al. (2008) Synaptotagmin VII regulates bone remodeling by modulating osteoclast and osteoblast secretion. Dev Cell 14: 914-25.
75. Jahn R, Scheller RH (2006) SNAREs-engines for membrane fusion. Nat Rev Mol Cell Biol 7: 631-643.
76. Chapman ER (2002) Synaptotagmin: a Ca(2+) sensor that triggers exocytosis? Nat Rev Mol Cell Biol 3: 498-508.
77. Verderio EA, Johnson T, Griffin M (2004) Tissue transglutaminase in normal and abnormal wound healing: review article. Amino Acids 26: 387-404.
78. Telci D, Griffin M (2006) Tissue transglutaminase (TG2)- a wound response enzyme. Front Biosci 11: 867-82.
79. Gundersen GG, Gomes ER, Wen Y (2004) Cortical control of microtubule stability and polarization. Curr Opin Cell Biol 16: 106-12.
80. Ádány R, Bárdos H (2003) Factor XIII subunit A as an intracellular transglutaminase. Cell Mol Life Sci 60: 1049-1060.
81. Paye M, Nusgens BV, Lapière CM (1989) Factor XIII of blood coagulation modulates collagen biosynthesis by fibroblasts in vitro. Haemostasis 19: 274-83.
82. Nahrendorf M, Hu K, Frantz S, Jaffer FA, Tung CH, et al. (2006) Factor XIII deficiency causes cardiac rupture, impairs wound healing, and aggravates cardiac remodeling in mice with myocardial infarction. Circulation 113: 1196-202.
83. Hsieh L, Nugent D (2008) Factor XIII deficiency. Haemophilia 14: 1190-200.
84. Inbal A, Lubetsky A, Krapp T, Castel D, Shaish A, et al. (2005) Impaired wound healing in factor XIII deficient mice. Thromb Haemost 94: 432-7.
85. Akimov SS, Belkin AM (2001) Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood 98: 1567-76.
86. Linder S, Hüfner K, Wintergerst U, Aepfelbacher M (2000) Microtubuledependent formation of podosomal adhesion structures in primary human macrophages. J Cell Sci 23: 4165-76.
87. Wolff J (2009) Plasma membrane tubulin. Bochim Biophys Acta 1788: 1415-1433.
88. Janich P, Corbeil D (2007) GM1 and GM3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells. FEBS Lett 581: 1783-7.
89. Gundersen GG, Cook TA (1999) Microtubules and signal transduction. Curr Opin Cell Biol 11: 81-94.
90. Gundersen GG (2002) Evolutionary conservation of microtubule-capture mechanisms. Nat Rev Mol Cell Biol 3: 296-304.
91. Mimori-Kiyosue Y, Tsukita S (2003) "Search and Capture" of microtubules through plus-end-binding proteins. J Biochem 134: 321-326.
92. Maccioni RB, Arechaga J (1986) Transglutaminase (TG) involvement in early embryogenesis. Exp Cell Res 167: 266-70.
93. Tucholski J, Kuret J, Johnson GV (1999) Tau is modified by tissue transglutaminase in situ: possible functional and metabolic effects of polyamination. J Neurochem 73: 1871-80.
94. Del Duca S, Serafini-Fracassini D, Bonner P, Cresti M, Cai G (2009) Effects of post-translational modifications catalysed by pollen transglutaminase on the functional properties of microtubules and actin filaments. Biochem J 418: 651-64.
95. Nakano Y, Addison WN, Kaartinen MT (2007) ATP mediated mineralization of MC3T3-E1 osteoblast cell cultures. Bone 41: 549-561.
96. Nakano Y, Forsprecher J, Kaartinen MT (2010) Regulation of ATPase activity of transglutaminase 2 by MT1-MMP - implications to mineralization of osteoblast cultures. J Cell Physiol 223: 260-269.
97. Kaverina I, Rottner K, Small JV (1998) Targeting, capture, and stabilization of microtubules at early focal adhesions. J Cell Biol 142: 181-90.
98. Wang D, Christensen K, Chawala K, Xiao G, Krebsbach PH, et al. (1999) Isolation and characterization of MC3T3-E1 preosteoblast subclones with distinct in vitro and in vivo differentiation/mineralization potential. J Bone Miner Res 9: 843-854.
99. Tullberg-Reinert H, Jundt G (1999) In situ measurement of collagen synthesis by human bone cells with a Sirius red-based colorimetric microassay: effects of transforming growth factor b2 and ascorbic 2-phosphate. Histochem Cell Biol 112: 271-276.
100. Sechler JL, Corbett SA, Schwarzbauer JE (1997) Modulatory roles for integrin activation and the synergy site of fibronectin during matrix assembly. Mol Biol Cell 8: 2563-73.
101. Ecarot-Charrier B, Glorieux FH, van der Rest M, Pereira G (1983) Osteoblasts isolated from mouse calvaria initiate matrix mineralization in culture. J Cell Biol 96: 639-643.