Choline kinase beta is required for normal endochondral bone formation

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 7, 2014, Pages 2112-2122

  Li, Zhuo ^a   Wu, Gengshu ^a   Sher, Roger B ^b   Khavandgar, Zohreh ^c   Hermansson, Martin ^a   Cox, Gregory A ^d   Doschak, Michael R ^a   Murshed, Monzur ^c   Beier, Frank ^e   Vance, Dennis E ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF MAINE   (United States)

^c MCGILL UNIVERSITY   (Canada)

^d JACKSON LABORATORY   (United States)

^e WESTERN UNIVERSITY   (Canada)

Author keywords

Choline kinase; Chondrocyte; Endochondral bone formation; Growth plate; Radius; Ulna

Indexed keywords

CHOLINE KINASE; CHOLINE KINASE BETA; COLLAGENASE 3; GELATINASE B; PHOSPHATIDYLCHOLINE; PHOSPHORYLCHOLINE; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE; BONE DEFORMATION; CARTILAGE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CHKB GENE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; ENCHONDRAL OSSIFICATION; GROWTH PLATE; HYPERTROPHY; MOUSE; NEWBORN; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIUS; ULNA; YOUNG ADULT;

CHOLINE KINASE; CHONDROCYTE; ENDOCHONDRAL BONE FORMATION; GROWTH PLATE; RADIUS; ULNA;

ANIMALS; CELL DIFFERENTIATION; CHOLINE KINASE; CHONDROCYTES; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FORELIMB; GROWTH PLATE; HUMANS; MICE; MICE, KNOCKOUT; OSTEOGENESIS; PHOSPHATIDYLCHOLINES;

EID: 84899873438     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.03.008     Document Type: Article

References (82)

1. D.E. Vance, and J.E. Vance Phospholipid biosynthesis in eukaryotes D.E. Vance, J.E. Vance, Biochemistry of Lipids, Lipoproteins, and Membranes 5th edition 2008 Elsevier Amsterdam 213 244
2. E.P. Kennedy Metabolism of lipides Annu. Rev. Biochem. 26 1957 119 148
3. J. Wittenberg, and A. Kornberg Choline phosphokinase J. Biol. Chem. 202 1953 431 444
4. C. Aoyama, H. Liao, and K. Ishidate Structure and function of choline kinase isoforms in mammalian cells Prog. Lipid Res. 43 2004 266 281
5. G. Wu, C. Aoyama, S.G. Young, and D.E. Vance Early embryonic lethality caused by disruption of the gene for choline kinase alpha, the first enzyme in phosphatidylcholine biosynthesis J. Biol. Chem. 283 2008 1456 1462
6. R.B. Sher, C. Aoyama, K.A. Huebsch, S. Ji, J. Kerner, Y. Yang, W.N. Frankel, C.L. Hoppel, P.A. Wood, D.E. Vance, and G.A. Cox A rostrocaudal muscular dystrophy caused by a defect in choline kinase beta, the first enzyme in phosphatidylcholine biosynthesis J. Biol. Chem. 281 2006 4938 4948
7. G. Wu, R.B. Sher, G.A. Cox, and D.E. Vance Understanding the muscular dystrophy caused by deletion of choline kinase beta in mice Biochim. Biophys. Acta 1791 2009 347 356
8. B.R. Olsen, A.M. Reginato, and W. Wang Bone development Annu. Rev. Cell Dev. Biol. 16 2000 191 220
9. G. Karsenty, and E.F. Wagner Reaching a genetic and molecular understanding of skeletal development Dev. Cell 2 2002 389 406
10. H.M. Kronenberg Developmental regulation of the growth plate Nature 423 2003 332 336
11. S. Provot, and E. Schipani Molecular mechanisms of endochondral bone development Biochem. Biophys. Res. Commun. 328 2005 658 665
12. E.J. Mackie, Y.A. Ahmed, L. Tatarczuch, K.S. Chen, and M. Mirams Endochondral ossification: how cartilage is converted into bone in the developing skeleton Int. J. Biochem. Cell Biol. 40 2008 46 62
13. W. Bi, J.M. Deng, Z. Zhang, R.R. Behringer, and B. de Crombrugghe Sox9 is required for cartilage formation Nat. Genet. 22 1999 85 89
14. H. Akiyama, M.C. Chaboissier, J.F. Martin, A. Schedl, and B. de Crombrugghe The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6 Genes Dev. 16 2002 2813 2828
15. T.H. Vu, J.M. Shipley, G. Bergers, J.E. Berger, J.A. Helms, D. Hanahan, S.D. Shapiro, R.M. Senior, and Z. Werb MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes Cell 93 1998 411 422
16. M. Inada, Y. Wang, M.H. Byrne, M.U. Rahman, C. Miyaura, C. Lopez-Otin, and S.M. Krane Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification Proc. Natl. Acad. Sci. U. S. A. 101 2004 17192 17197
17. D. Stickens, D.J. Behonick, N. Ortega, B. Heyer, B. Hartenstein, Y. Yu, A.J. Fosang, M. Schorpp-Kistner, P. Angel, and Z. Werb Altered endochondral bone development in matrix metalloproteinase 13-deficient mice Development 131 2004 5883 5895
18. N. Ortega, D. Behonick, D. Stickens, and Z. Werb How proteases regulate bone morphogenesis Ann. N. Y. Acad. Sci. 995 2003 109 116
19. N. Ortega, D.J. Behonick, and Z. Werb Matrix remodeling during endochondral ossification Trends Cell Biol. 14 2004 86 93
20. R.T. Ballock, and R.J. O'Keefe Physiology and pathophysiology of the growth plate Birth Defects Res. C Embryo Today 69 2003 123 143
21. F. Beier Cell-cycle control and the cartilage growth plate J. Cell. Physiol. 202 2005 1 8
22. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
23. G. Wang, A. Woods, H. Agoston, V. Ulici, M. Glogauer, and F. Beier Genetic ablation of Rac1 in cartilage results in chondrodysplasia Dev. Biol. 306 2007 612 623
24. V. Ulici, K.D. Hoenselaar, H. Agoston, D.D. McErlain, J. Umoh, S. Chakrabarti, D.W. Holdsworth, and F. Beier The role of Akt1 in terminal stages of endochondral bone formation: angiogenesis and ossification Bone 45 2009 1133 1145
25. S.E. Usmani, M.A. Pest, G. Kim, S.N. Ohora, L. Qin, and F. Beier Transforming growth factor alpha controls the transition from hypertrophic cartilage to bone during endochondral bone growth Bone 51 2012 131 141
26. C.G. James, A. Woods, T.M. Underhill, and F. Beier The transcription factor ATF3 is upregulated during chondrocyte differentiation and represses cyclin D1 and A gene transcription BMC Mol. Biol. 7 2006 30
27. K. Ishidate, and Y. Nakazawa Choline/ethanolamine kinase from rat kidney Methods Enzymol. 209 1992 121 134
28. J. Folch, M. Lees, and G.H. Sloane Stanley A simple method for the isolation and purification of total lipides from animal tissues J. Biol. Chem. 226 1957 497 509
29. M. Hermansson, A. Uphoff, R. Kakela, and P. Somerharju Automated quantitative analysis of complex lipidomes by liquid chromatography/mass spectrometry Anal. Chem. 77 2005 2166 2175
30. V. Kainu, M. Hermansson, and P. Somerharju Electrospray ionization mass spectrometry and exogenous heavy isotope-labeled lipid species provide detailed information on aminophospholipid acyl chain remodeling J. Biol. Chem. 283 2008 3676 3687
31. Y. Xiong, Y.Y. Zhao, S. Goruk, K. Oilund, C.J. Field, R.L. Jacobs, and J.M. Curtis Validation of an LC-MS/MS method for the quantification of choline-related compounds and phospholipids in foods and tissues J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 911 2012 170 179
32. J. Baker, J.P. Liu, E.J. Robertson, and A. Efstratiadis Role of insulin-like growth factors in embryonic and postnatal growth Cell 75 1993 73 82
33. S. Yakar, C.J. Rosen, W.G. Beamer, C.L. Ackert-Bicknell, Y. Wu, J.L. Liu, G.T. Ooi, J. Setser, J. Frystyk, Y.R. Boisclair, and D. LeRoith Circulating levels of IGF-1 directly regulate bone growth and density J. Clin. Invest. 110 2002 771 781
34. S.M. Krane, and M. Inada Matrix metalloproteinases and bone Bone 43 2008 7 18
35. D.V. Novack, and S.L. Teitelbaum The osteoclast: friend or foe? Annu. Rev. Pathol. 3 2008 457 484
36. N. Ortega, K. Wang, N. Ferrara, Z. Werb, and T.H. Vu Complementary interplay between matrix metalloproteinase-9, vascular endothelial growth factor and osteoclast function drives endochondral bone formation Dis. Model Mech. 3 2010 224 235
37. T. Yoshida, and P.H. Stern How vitamin D works on bone Endocrinol. Metab. Clin. North Am. 41 2012 557 569
38. S. Mitsuhashi, and I. Nishino Megaconial congenital muscular dystrophy due to loss-of-function mutations in choline kinase beta Curr. Opin. Neurol. 26 2013 536 543
39. E. Rao, B. Weiss, M. Fukami, A. Rump, B. Niesler, A. Mertz, K. Muroya, G. Binder, S. Kirsch, M. Winkelmann, G. Nordsiek, U. Heinrich, M.H. Breuning, M.B. Ranke, A. Rosenthal, T. Ogata, and G.A. Rappold Pseudoautosomal deletions encompassing a novel homeobox gene cause growth failure in idiopathic short stature and Turner syndrome Nat. Genet. 16 1997 54 63
40. C.F. Munns, I.A. Glass, R. LaBrom, M. Hayes, S. Flanagan, M. Berry, V.J. Hyland, J.A. Batch, G.E. Philips, and D. Vickers Histopathological analysis of Leri-Weill dyschondrosteosis: disordered growth plate Hand Surg. 6 2001 13 23
41. A.R. Zinn, F. Wei, L. Zhang, F.F. Elder, C.I. Scott Jr., P. Marttila, and J.L. Ross Complete SHOX deficiency causes Langer mesomelic dysplasia Am. J. Med. Genet. 110 2002 158 163
42. F. Gianfrancesco, R. Sanges, T. Esposito, S. Tempesta, E. Rao, G. Rappold, N. Archidiacono, J.A. Graves, A. Forabosco, and M. D'Urso Differential divergence of three human pseudoautosomal genes and their mouse homologs: implications for sex chromosome evolution Genome Res. 11 2001 2095 2100
43. M. Clement-Jones, S. Schiller, E. Rao, R.J. Blaschke, A. Zuniga, R. Zeller, S.C. Robson, G. Binder, I. Glass, T. Strachan, S. Lindsay, and G.A. Rappold The short stature homeobox gene SHOX is involved in skeletal abnormalities in Turner syndrome Hum. Mol. Genet. 9 2000 695 702
44. J. Cobb, A. Dierich, Y. Huss-Garcia, and D. Duboule A mouse model for human short-stature syndromes identifies Shox2 as an upstream regulator of Runx2 during long-bone development Proc. Natl. Acad. Sci. U. S. A. 103 2006 4511 4515
45. L. Yu, H. Liu, M. Yan, J. Yang, F. Long, K. Muneoka, and Y. Chen Shox2 is required for chondrocyte proliferation and maturation in proximal limb skeleton Dev. Biol. 306 2007 549 559
46. L. Vickerman, S. Neufeld, and J. Cobb Shox2 function couples neural, muscular and skeletal development in the proximal forelimb Dev. Biol. 350 2011 323 336
47. R. Zeller, J. Lopez-Rios, and A. Zuniga Vertebrate limb bud development: moving towards integrative analysis of organogenesis Nat. Rev. Genet. 10 2009 845 858
48. A.P. Davis, D.P. Witte, H.M. Hsieh-Li, S.S. Potter, and M.R. Capecchi Absence of radius and ulna in mice lacking hoxa-11 and hoxd-11 Nature 375 1995 791 795
49. A.M. Boulet, and M.R. Capecchi Multiple roles of Hoxa11 and Hoxd11 in the formation of the mammalian forelimb zeugopod Development 131 2004 299 309
50. L. Blavier, and J.M. Delaisse Matrix metalloproteinases are obligatory for the migration of preosteoclasts to the developing marrow cavity of primitive long bones J. Cell Sci. 108 Pt 12 1995 3649 3659
51. M.T. Engsig, Q.J. Chen, T.H. Vu, A.C. Pedersen, B. Therkidsen, L.R. Lund, K. Henriksen, T. Lenhard, N.T. Foged, Z. Werb, and J.M. Delaisse Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones J. Cell Biol. 151 2000 879 889
52. W. Bi, W. Huang, D.J. Whitworth, J.M. Deng, Z. Zhang, R.R. Behringer, and B. de Crombrugghe Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization Proc. Natl. Acad. Sci. U. S. A. 98 2001 6698 6703
53. J.C. Lacal Choline kinase: a novel target for antitumor drugs IDrugs 4 2001 419 426
54. A. Rodriguez-Gonzalez, A. Ramirez de Molina, J. Benitez-Rajal, and J.C. Lacal Phospholipase D and choline kinase: their role in cancer development and their potential as drug targets Prog. Cell Cycle Res. 5 2003 191 201
55. K. Glunde, Z.M. Bhujwalla, and S.M. Ronen Choline metabolism in malignant transformation Nat. Rev. Cancer 11 2011 835 848
56. D. Gallego-Ortega, T. Gomez del Pulgar, F. Valdes-Mora, A. Cebrian, and J.C. Lacal Involvement of human choline kinase alpha and beta in carcinogenesis: a different role in lipid metabolism and biological functions Adv. Enzyme Regul. 51 2011 183 194
57. A. Cuadrado, A. Carnero, F. Dolfi, B. Jimenez, and J.C. Lacal Phosphorylcholine: a novel second messenger essential for mitogenic activity of growth factors Oncogene 8 1993 2959 2968
58. B. Jimenez, L. del Peso, S. Montaner, P. Esteve, and J.C. Lacal Generation of phosphorylcholine as an essential event in the activation of Raf-1 and MAP-kinases in growth factors-induced mitogenic stimulation J. Cell. Biochem. 57 1995 141 149
59. Z. Kiss, and T. Chung Choline phosphate and phorbol ester potentiate the mitogenic effect of insulin by competitive mechanisms in NIH 3 T3 fibroblasts Biochem. Biophys. Res. Commun. 218 1996 505 509
60. K. Nakagami, T. Uchida, S. Ohwada, Y. Koibuchi, Y. Suda, T. Sekine, and Y. Morishita Increased choline kinase activity and elevated phosphocholine levels in human colon cancer Jpn. J. Cancer Res. 90 1999 419 424
61. A. Ramirez de Molina, A. Rodriguez-Gonzalez, R. Gutierrez, L. Martinez-Pineiro, J. Sanchez, F. Bonilla, R. Rosell, and J. Lacal Overexpression of choline kinase is a frequent feature in human tumor-derived cell lines and in lung, prostate, and colorectal human cancers Biochem. Biophys. Res. Commun. 296 2002 580 583
62. A. Ramirez de Molina, J. Sarmentero-Estrada, C. Belda-Iniesta, M. Taron, V. Ramirez de Molina, P. Cejas, M. Skrzypski, D. Gallego-Ortega, J. de Castro, E. Casado, M.A. Garcia-Cabezas, J.J. Sanchez, M. Nistal, R. Rosell, M. Gonzalez-Baron, and J.C. Lacal Expression of choline kinase alpha to predict outcome in patients with early-stage non-small-cell lung cancer: a retrospective study Lancet Oncol. 8 2007 889 897
63. G. Eliyahu, T. Kreizman, and H. Degani Phosphocholine as a biomarker of breast cancer: molecular and biochemical studies Int. J. Cancer 120 2007 1721 1730
64. G. Wu, R.B. Sher, G.A. Cox, and D.E. Vance Differential expression of choline kinase isoforms in skeletal muscle explains the phenotypic variability in the rostrocaudal muscular dystrophy mouse Biochim. Biophys. Acta 1801 2010 446 454
65. C. Kent Regulation of phosphatidylcholine biosynthesis Prog. Lipid Res. 29 1990 87 105
66. D.E. Vance Boehringer Mannheim Award lecture. Phosphatidylcholine metabolism: masochistic enzymology, metabolic regulation, and lipoprotein assembly Biochem. Cell Biol. 68 1990 1151 1165
67. B. Houston, A.J. Stewart, and C. Farquharson PHOSPHO1 - A novel phosphatase specifically expressed at sites of mineralisation in bone and cartilage Bone 34 2004 629 637
68. A.J. Stewart, S.J. Roberts, E. Seawright, M.G. Davey, R.H. Fleming, and C. Farquharson The presence of PHOSPHO1 in matrix vesicles and its developmental expression prior to skeletal mineralization Bone 39 2006 1000 1007
69. S. Roberts, S. Narisawa, D. Harmey, J.L. Millan, and C. Farquharson Functional involvement of PHOSPHO1 in matrix vesicle-mediated skeletal mineralization J. Bone Miner. Res. 22 2007 617 627
70. M.C. Yadav, A.M. Simao, S. Narisawa, C. Huesa, M.D. McKee, C. Farquharson, and J.L. Millan 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. 26 2011 286 297
71. S.J. Roberts, A.J. Stewart, P.J. Sadler, and C. Farquharson Human PHOSPHO1 exhibits high specific phosphoethanolamine and phosphocholine phosphatase activities Biochem. J. 382 2004 59 65
72. S.J. Roberts, A.J. Stewart, R. Schmid, C.A. Blindauer, S.R. Bond, P.J. Sadler, and C. Farquharson Probing the substrate specificities of human PHOSPHO1 and PHOSPHO2 Biochim. Biophys. Acta 1752 2005 73 82
73. B.J. Kvam, P. Pollesello, F. Vittur, and S. Paoletti 31P NMR studies of resting zone cartilage from growth plate Magn. Reson. Med. 25 1992 355 361
74. T.J. Porter, and C. Kent Purification and characterization of choline/ethanolamine kinase from rat liver J. Biol. Chem. 265 1990 414 422
75. C. Aoyama, K. Nakashima, and K. Ishidate Molecular cloning of mouse choline kinase and choline/ethanolamine kinase: their sequence comparison to the respective rat homologs Biochim. Biophys. Acta 1393 1998 179 185
76. D.W. Moss, R.H. Eaton, J.K. Smith, and L.G. Whitby Association of inorganic-pyrophosphatase activity with human alkaline-phosphatase preparations Biochem. J. 102 1967 53 57
77. R.J. Majeska, and R.E. Wuthier Studies on matrix vesicles isolated from chick epiphyseal cartilage. Association of pyrophosphatase and ATPase activities with alkaline phosphatase Biochim. Biophys. Acta 391 1975 51 60
78. H.C. Anderson Molecular biology of matrix vesicles Clin. Orthop. Relat. Res. 1995 266 280
79. I. Aubin, C.P. Adams, S. Opsahl, D. Septier, C.E. Bishop, N. Auge, R. Salvayre, A. Negre-Salvayre, M. Goldberg, J.L. Guenet, and C. Poirier A deletion in the gene encoding sphingomyelin phosphodiesterase 3 (Smpd3) results in osteogenesis and dentinogenesis imperfecta in the mouse Nat. Genet. 37 2005 803 805
80. W. Stoffel, B. Jenke, B. Block, M. Zumbansen, and J. Koebke Neutral sphingomyelinase 2 (smpd3) in the control of postnatal growth and development Proc. Natl. Acad. Sci. U. S. A. 102 2005 4554 4559
81. W. Stoffel, B. Jenke, B. Holz, E. Binczek, R.H. Gunter, J. Knifka, J. Koebke, and A. Niehoff Neutral sphingomyelinase (SMPD3) deficiency causes a novel form of chondrodysplasia and dwarfism that is rescued by Col2A1-driven smpd3 transgene expression Am. J. Pathol. 171 2007 153 161
82. Z. Khavandgar, C. Poirier, C.J. Clarke, J. Li, N. Wang, M.D. McKee, Y.A. Hannun, and M. Murshed A cell-autonomous requirement for neutral sphingomyelinase 2 in bone mineralization J. Cell Biol. 194 2011 277 289