Critical role of filamin-binding LIM protein 1 (FBLP-1)/migfilin in regulation of bone remodeling

Journal of Biological Chemistry

Volumn 287, Issue 25, 2012, Pages 21450-21460

  Xiao, Guozhi ^a,b   Cheng, Hongqiang ^c,d   Cao, Huiling ^a   Chen, Ka ^a   Tu, Yizeng ^a   Yu, Shibing ^a   Jiao, Hongli ^a,b   Yang, Shengyong ^a   Im, Hee Jeong ^b   Chen, Di ^b   Chen, Ju ^c   Wu, Chuanyue ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BONE HOMEOSTASIS; BONE MARROW; BONE MARROW STROMAL CELLS; BONE REMODELING; COMPLEX PROCESSES; EXTRACELLULAR MATRICES; FOCAL ADHESIONS; IN-VITRO; IN-VIVO; INTRINSIC PROPERTY; KEY REGULATORS; NUCLEAR FACTORS; OSTEOCLASTOGENESIS; RECEPTOR ACTIVATOR; WILD TYPES;

ADHESION; CHEMICAL ACTIVATION; GENE ENCODING; PHOSPHORYLATION; PROTEINS;

BONE;

FILAMIN BINDING LIM PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OSTEOCLAST DIFFERENTIATION FACTOR; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE REMODELING; CELL ADHESION; CELL COMMUNICATION; CELL COUNT; CELL DIFFERENTIATION; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; DISEASE SEVERITY; EMBRYO; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; FEMALE; FILAMIN BINDING LIM PROTEIN 1 GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETIC CODE; IN VITRO STUDY; IN VIVO STUDY; MALE; MONOCYTE; MOUSE; MULTINUCLEAR CELL; NONHUMAN; OSTEOBLAST; OSTEOCLAST ACTIVITY; OSTEOCLASTOGENESIS; OSTEOPENIA; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATOR GENE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STROMA CELL; WILD TYPE;

ANIMALS; BONE MARROW CELLS; BONE REMODELING; CELL ADHESION; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELL MOVEMENT; CYTOSKELETAL PROTEINS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 3; MONOCYTES; OSTEOBLASTS; OSTEOCLASTS; PHOSPHORYLATION; STROMAL CELLS;

EID: 84862275091     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.331249     Document Type: Article

References (57)

1. Ash, P., Loutit, J. F., and Townsend, K. M. (1980) Osteoclasts derived from haematopoietic stem cells. Nature 283, 669-670 (Pubitemid 10099996)
2. Lacey, D. L., Timms, E., Tan, H. L., Kelley, M. J., Dunstan, C. R., Burgess, T., Elliott, R., Colombero, A., Elliott, G., Scully, S., Hsu, H., Sullivan, J., Hawkins, N., Davy, E., Capparelli, C., Eli, A., Qian, Y. X., Kaufman, S., Sarosi, I., Shalhoub, V., Senaldi, G., Guo, J., Delaney, J., and Boyle, W. J. (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93, 165-176 (Pubitemid 28180851)
3. Yasuda, H., Shima, N., Nakagawa, N., Yamaguchi, K., Kinosaki, M., Mochizuki, S., Tomoyasu, A., Yano, K., Goto, M., Murakami, A., Tsuda, E., Morinaga, T., Higashio, K., Udagawa, N., Takahashi, N., and Suda, T. (1998) Osteoclast differentiation factor is a ligand for osteoprotegerin/ osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc. Natl. Acad. Sci. U.S.A. 95, 3597-3602
4. Simonet, W. S., Lacey, D. L., Dunstan, C. R., Kelley, M., Chang, M. S., Lüthy, R., Nguyen, H. Q., Wooden, S., Bennett, L., Boone, T., Shimamoto, G., DeRose, M., Elliott, R., Colombero, A., Tan, H. L., Trail, G., Sullivan, J., Davy, E., Bucay, N., Renshaw-Gegg, L., Hughes, T. M., Hill, D., Pattison, W., Campbell, P., Sander, S., Van, G., Tarpley, J., Derby, P., Lee, R., and Boyle, W. J. (1997) Osteoprotegerin. A novel secreted protein involved in the regulation of bone density. Cell 89, 309-319 (Pubitemid 27199902)
5. O'Brien, C. A. (2010) Control of RANKL gene expression. Bone 46, 911-919
6. Boyle, W. J., Simonet, W. S., and Lacey, D. L. (2003) Osteoclast differentiation and activation. Nature 423, 337-342 (Pubitemid 40852708)
7. Asagiri, M., and Takayanagi, H. (2007) The molecular understanding of osteoclast differentiation. Bone 40, 251-264 (Pubitemid 46054562)
8. Yavropoulou, M. P., and Yovos, J. G. (2008) Osteoclastogenesis. Current knowledge and future perspectives. J. Musculoskelet. Neuronal Interact. 8, 204-216
9. Roodman, G. D., and Windle, J. J. (2005) Paget disease of bone. J. Clin. Invest. 115, 200-208 (Pubitemid 40385458)
10. Matsuo, K., and Irie, N. (2008) Osteoclast-osteoblast communication. Arch. Biochem. Biophys 473, 201-209
11. Sims, N. A., and Gooi, J. H. (2008) Bone remodeling. Multiple cellular interactions required for coupling of bone formation and resorption. Semin. Cell Dev. Biol. 19, 444-451
12. Henriksen, K., Neutzsky-Wulff, A. V., Bonewald, L. F., and Karsdal, M. A. (2009) Local communication on and within bone controls bone remodeling. Bone 44, 1026-1033
13. Nakahama, K. (2010) Cellular communications in bone homeostasis and repair. Cell Mol. Life Sci. 67, 4001-4009
14. Cao, X. (2011) Targeting osteoclast-osteoblast communication. Nat. Med. 17, 1344-1346
15. Tu, Y., Wu, S., Shi, X., Chen, K., and Wu, C. (2003) Migfilin and Mig-2 link focal adhesions to filamin and the actin cytoskeleton and function in cell shape modulation. Cell 113, 37-47 (Pubitemid 36411958)
16. Larjava, H., Plow, E. F., and Wu, C. (2008) Kindlins. Essential regulators of integrin signalling and cell-matrix adhesion. EMBO Rep. 9, 1203-1208
17. Meves, A., Stremmel, C., Gottschalk, K., and Fässler, R. (2009) The Kindlin protein family. New members to the club of focal adhesion proteins. Trends Cell Biol. 19, 504-513
18. Moser, M., Legate, K. R., Zent, R., and Fässler, R. (2009) The tail of integrins, talin, and kindlins. Science 324, 895-899
19. Plow, E. F., Qin, J., and Byzova, T. (2009) Kindling the flame of integrin activation and function with kindlins. Curr. Opin. Hematol. 16, 323-328
20. Lai-Cheong, J. E., Parsons, M., and McGrath, J. A. (2010) The role of kindlins in cell biology and relevance to human disease. Int. J. Biochem. Cell Biol. 42, 595-603
21. Wu, C. (2005) Migfilin and its binding partners. From cell biology to human diseases. J. Cell Sci. 118, 659-664
22. Zhang, Y., Tu, Y., Gkretsi, V., and Wu, C. (2006) Migfilin interacts with vasodilator-stimulated phosphoprotein (VASP) and regulates VASP localization to cell-matrix adhesions and migration. J. Biol. Chem. 281, 12397-12407 (Pubitemid 43855324)
23. Gkretsi, V., Zhang, Y., Tu, Y., Chen, K., Stolz, D. B., Yang, Y., Watkins, S. C., and Wu, C. (2005) Physical and functional association of migfilin with cell-cell adhesions. J. Cell Sci. 118, 697-710 (Pubitemid 40372579)
24. Lad, Y., Jiang, P., Ruskamo, S., Harburger, D. S., Ylänne, J., Campbell, I. D., and Calderwood, D. A. (2008) Structural basis of the migfilin-filamin interaction and competition with integrin β tails. J. Biol. Chem. 283, 35154-35163
25. Lai-Cheong, J. E., Ussar, S., Arita, K., Hart, I. R., and McGrath, J. A. (2008) Colocalization of kindlin-1, kindlin-2, and migfilin at keratinocyte focal adhesion and relevance to the pathophysiology of Kindler syndrome. J. Invest. Dermatol. 128, 2156-2165
26. Ithychanda, S. S., Das, M., Ma, Y. Q., Ding, K., Wang, X., Gupta, S., Wu, C., Plow, E. F., and Qin, J. (2009) Migfilin, a molecular switch in regulation of integrin activation. J. Biol. Chem. 284, 4713-4722
27. Zhao, J., Zhang, Y., Ithychanda, S. S., Tu, Y., Chen, K., Qin, J., and Wu, C. (2009) Migfilin interacts with Src and contributes to cell-matrix adhesion-mediated survival signaling. J. Biol. Chem. 284, 34308-34320
28. Das, M., Ithychanda, S. S., Qin, J., and Plow, E. F. (2011) Migfilin and filamin as regulators of integrin activation in endothelial cells and neutrophils. PLoS One 6, e26355
29. Ithychanda, S. S., and Qin, J. (2011) Evidence for multisite ligand binding and stretching of filamin by integrin and migfilin. Biochemistry 50, 4229-4231
30. Liang, X., Zhou, Q., Li, X., Sun, Y., Lu, M., Dalton, N., Ross, J., Jr., and Chen, J. (2005) PINCH1 plays an essential role in early murine embryonic development but is dispensable in ventricular cardiomyocytes. Mol. Cell. Biol. 25, 3056-3062 (Pubitemid 40464309)
31. Cheng, H., Kimura, K., Peter, A. K., Cui, L., Ouyang, K., Shen, T., Liu, Y., Gu, Y., Dalton, N. D., Evans, S. M., Knowlton, K. U., Peterson, K. L., and Chen, J. (2010) Loss of enigma homolog protein results in dilated cardiomyopathy. Circ. Res. 107, 348-356
32. O'Gorman, S., Dagenais, N. A., Qian, M., and Marchuk, Y. (1997) Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 94, 14602-14607 (Pubitemid 28041420)
33. Cao, H., Yu, S., Yao, Z., Galson, D. L., Jiang, Y., Zhang, X., Fan, J., Lu, B., Guan, Y., Luo, M., Lai, Y., Zhu, Y., Kurihara, N., Patrene, K., Roodman, G. D., and Xiao, G. (2010) Activating transcription factor 4 regulates osteoclast differentiation in mice. J. Clin. Invest. 120, 2755-2766
34. Yu, S., Franceschi, R. T., Luo, M., Fan, J., Jiang, D., Cao, H., Kwon, T. G., Lai, Y., Zhang, J., Patrene, K., Hankenson, K., Roodman, G. D., and Xiao, G. (2009) Critical role of activating transcription factor 4 in the anabolic actions of parathyroid hormone in bone. PLoS One 4, e7583
35. Yu, S., Franceschi, R. T., Luo, M., Zhang, X., Jiang, D., Lai, Y., Jiang, Y., Zhang, J., and Xiao, G. (2008) Parathyroid hormone increases activating transcription factor 4 expression and activity in osteoblasts. Requirement for osteocalcin gene expression. Endocrinology 149, 1960-1968 (Pubitemid 351468354)
36. Yu, S., Jiang, Y., Galson, D. L., Luo, M., Lai, Y., Lu, Y., Ouyang, H. J., Zhang, J., and Xiao, G. (2008) General transcription factor IIA-γ increases osteoblast- specific osteocalcin gene expression via activating transcription factor 4 and runt-related transcription factor 2. J. Biol. Chem. 283, 5542-5553
37. Xiao, G., Jiang, D., Gopalakrishnan, R., and Franceschi, R. T. (2002) Fibroblast growth factor 2 induction of the osteocalcin gene requires MAPK activity and phosphorylation of the osteoblast transcription factor, Cbfa1/Runx2. J. Biol. Chem. 277, 36181-36187
38. Qu, H., Tu, Y., Shi, X., Larjava, H., Saleem, M. A., Shattil, S. J., Fukuda, K., Qin, J., Kretzler, M., and Wu, C. (2011) Kindlin-2 regulates podocyte adhesion and fibronectin matrix deposition through interactions with phosphoinositides and integrins. J. Cell Sci. 124, 879-891
39. Shi, X., Ma, Y. Q., Tu, Y., Chen, K., Wu, S., Fukuda, K., Qin, J., Plow, E. F., and Wu, C. (2007) The MIG-2/integrin interaction strengthens cell-matrix adhesion and modulates cell motility. J. Biol. Chem. 282, 20455-20466 (Pubitemid 47100027)
40. Zhang, Y., Guo, L., Chen, K., and Wu, C. (2002) A critical role of the PINCH-integrin-linked kinase interaction in the regulation of cell shape change and migration. J. Biol. Chem. 277, 318-326 (Pubitemid 34952061)
41. Xiao, G., Cui, Y., Ducy, P., Karsenty, G., and Franceschi, R. T. (1997) Ascorbic acid-dependent activation of the osteocalcin promoter in MC3T3-E1 preosteoblasts. Requirement for collagen matrix synthesis and the presence of an intact OSE2 sequence. Mol. Endocrinol. 11, 1103-1113 (Pubitemid 27278833)
42. Singha, U. K., Jiang, Y., Yu, S., Luo, M., Lu, Y., Zhang, J., and Xiao, G. (2008) Rapamycin inhibits osteoblast proliferation and differentiation in MC3T3-E1 cells and primary mouse bone marrow stromal cells. J. Cell. Biochem. 103, 434-446 (Pubitemid 351171915)
43. Termine, J. D. (1990) Cellular activity, matrix proteins, and aging bone. Exp. Gerontol. 25, 217-221
44. Moursi, A. M., Damsky, C. H., Lull, J., Zimmerman, D., Doty, S. B., Aota, S., and Globus, R. K. (1996) Fibronectin regulates calvarial osteoblast differentiation. J. Cell Sci. 109, 1369-1380 (Pubitemid 26190487)
45. 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. Hum. Mutat. 28, 209-221
46. Shekaran, A., and García, A. J. (2011) Extracellular matrix-mimetic adhesive biomaterials for bone repair. J. Biomed. Mater. Res. A 96, 261-272
47. Siebers, M. C., ter Brugge, P. J., Walboomers, X. F., and Jansen, J. A. (2005) Integrins as linker proteins between osteoblasts and bone replacing materials. A critical review. Biomaterials 26, 137-146 (Pubitemid 38789096)
48. Nishida, S., Tsubaki, M., Hoshino, M., Namimatsu, A., Uji, H., Yoshioka, S., Tanimori, Y., Yanae, M., Iwaki, M., and Irimajiri, K. (2005) Nitrogencontaining bisphosphonate, YM529/ONO-5920 (a novel minodronic acid), inhibits RANKL expression in a cultured bone marrow stromal cell line ST2. Biochem. Biophys. Res. Commun. 328, 91-97 (Pubitemid 40164640)
49. Matsushita, T., Chan, Y. Y., Kawanami, A., Balmes, G., Landreth, G. E., and Murakami, S. (2009) Extracellular signal-regulated kinase 1 (ERK1) and ERK2 play essential roles in osteoblast differentiation and in supporting osteoclastogenesis. Mol. Cell. Biol. 29, 5843-5857
50. Walker, C. G., Dangaria, S., Ito, Y., Luan, X., and Diekwisch, T. G. (2010) Osteopontin is required for unloading-induced osteoclast recruitment and modulation of RANKL expression during tooth drift-associated bone remodeling, but not for super-eruption. Bone 47, 1020-1029
51. Lee, J. H., Kim, H. N., Yang, D., Jung, K., Kim, H. M., Kim, H. H., Ha, H., and Lee, Z. H. (2009) Trolox prevents osteoclastogenesis by suppressing RANKL expression and signaling. J. Biol. Chem. 284, 13725-13734
52. Moik, D. V., Janbandhu, V. C., and Fässler, R. (2011) Loss of migfilin expression has no overt consequences on murine development and homeostasis. J. Cell Sci. 124, 414-421
53. Brunner, M., Millon-Frémillon, A., Chevalier, G., Nakchbandi, I. A., Mosher, D., Block, M. R., Albigès-Rizo, C., and Bouvard, D. (2011) Osteoblast mineralization requires β1 integrin/ICAP-1-dependent fibronectin deposition. J. Cell Biol. 194, 307-322
54. Feng, Y., and Walsh, C. A. (2004) The many faces of filamin. A versatile molecular scaffold for cell motility and signalling. Nat. Cell Biol. 6, 1034-1038 (Pubitemid 39468003)
55. Hart, A. W., Morgan, J. E., Schneider, J., West, K., McKie, L., Bhattacharya, S., Jackson, I. J., and Cross, S. H. (2006) Cardiac malformations and midline skeletal defects in mice lacking filamin A. Hum. Mol. Genet. 15, 2457-2467 (Pubitemid 44288699)
56. Zhou, X., Tian, F., Sandzén, J., Cao, R., Flaberg, E., Szekely, L., Cao, Y., Ohlsson, C., Bergo, M. O., Borén, J., and Akyürek, L. M. (2007) Filamin B deficiency in mice results in skeletal malformations and impaired microvascular development. Proc. Natl. Acad. Sci. U.S.A. 104, 3919-3924 (Pubitemid 47181554)
57. Camacho, C. L. (2011) A New Role for Filamin A as a Regulator of Runx2 Function. Doctoral dissertation, University of Manchester, Manchester, UK