Genetic deletion of catalytic subunits of AMP-activated protein kinase increases osteoclasts and reduces bone mass in young adult mice

Journal of Biological Chemistry

Volumn 288, Issue 17, 2013, Pages 12187-12196

  Kang, Heeseog ^a   Viollet, Benoit ^b,c,d   Wu, Dianqing ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUT COCHIN   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMP-ACTIVATED PROTEIN KINASE; CATALYTIC SUBUNITS; ENERGY HOMEOSTASIS; HISTOMORPHOMETRIC ANALYSIS; METABOLIC DISORDERS; OSTEOCLASTOGENESIS; STATIC AND DYNAMIC; THERAPEUTIC TARGETS;

MAMMALS; PHYSIOLOGY;

BONE;

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA2; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MASS; BONE METABOLISM; BONE REMODELING; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; GENE DELETION; IN VITRO STUDY; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; OSSIFICATION; OSTEOCLASTOGENESIS; OSTEOLYSIS; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WILD TYPE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BONE AND BONES; BONE RESORPTION; MICE; MICE, KNOCKOUT; ORGAN SIZE; OSTEOCLASTS; OSTEOGENESIS; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; SIGNAL TRANSDUCTION;

MAMMALIA; MUS;

EID: 84876944006     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.430389     Document Type: Article

References (48)

1. Kemp, B. E., Mitchelhill, K. I., Stapleton, D., Michell, B. J., Chen, Z. P., and Witters, L. A. (1999) Dealing with energy demand. The AMP-activated protein kinase. Trends Biochem. Sci. 24, 22-25
2. Davies, S. P., Carling, D., and Hardie, D. G. (1989) Tissue distribution of the AMP-activated protein kinase, and lack of activation by cyclic-AMP-dependent protein kinase, studied using a specific and sensitive peptide assay. Eur. J. Biochem. 186, 123-128
3. Birk, J. B., and Wojtaszewski, J. F. (2006) Predominant a2/j32/y3 AMPK activation during exercise in human skeletal muscle. J. Physiol. 577, 1021-1032
4. Mahlapuu, M., Johansson, C., Lindgren, K., Hjälm, G., Barnes, B. R., Krook, A., Zierath, J. R., Andersson, L., and Marklund, S. (2004) Expression profiling of the 7-subunit isoforms of AMP-activated protein kinase suggests a major role for 73 in white skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 286, E194-E200
5. Ingebritsen, T. S., Lee, H. S., Parker, R. A., and Gibson, D. M. (1978) Reversible modulation of the activities of both liver microsomal hydroxymethylglutaryl coenzyme A reductase and its inactivating enzyme. Evidence for regulation by phosphorylation-dephosphorylation. Biochem. Biophys. Res. Commun. 81, 1268-1277
6. Karsenty, G. (2006) Convergence between bone and energy homeostases. Leptin regulation of bone mass. Cell Metab. 4, 341-348
7. Yadav, V. K., Oury, F., Suda, N., Liu, Z. W., Gao, X. B., Confavreux, C., Klemenhagen, K. C., Tanaka, K. F., Gingrich, J. A., Guo, X. E., Tecott, L. H., Mann, J. J., Hen, R., Horvath, T. L., and Karsenty, G. (2009) A serotonindependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure. Cell 138, 976-989
8. Ducy, P., Amling, M., Takeda, S., Priemel, M., Schilling, A. F., Beil, F. T., Shen, J., Vinson, C., Rueger, J. M., and Karsenty, G. (2000) Leptin inhibits bone formation through a hypothalamic relay. A central control of bone mass. Cell 100, 197-207
9. Takeda, S., Elefteriou, F., Levasseur, R., Liu, X., Zhao, L., Parker, K. L., Armstrong, D., Ducy, P., and Karsenty, G. (2002) Leptin regulates bone formation via the sympathetic nervous system. Cell 111, 305-317
10. Ferron, M., Wei, J., Yoshizawa, T., Del Fattore, A., DePinho, R. A., Teti, A., Ducy, P., and Karsenty, G. (2010) Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 142, 296-308
11. Fulzele, K., Riddle, R. C., DiGirolamo, D. J., Cao, X., Wan, C., Chen, D., Faugere, M. C., Aja, S., Hussain, M. A., Brüning, J. C., and Clemens, T. L. (2010) Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell 142, 309-319
12. Jeyabalan, J., Shah, M., Viollet, B., and Chenu, C (2012) AMP-activated protein kinase pathway and bone metabolism. J. Endocrinol. 212, 277-290
13. Kasai, T., Bandow, K., Suzuki, H., Chiba, N., Kakimoto, K., Ohnishi, T., Kawamoto, S., Nagaoka, E., and Matsuguchi, T. (2009) Osteoblast differentiation is functionally associated with decreased AMP kinase activity. J. Cell Physiol. 221, 740-749
14. Quinn, J. M., Tam, S., Sims, N. A., Saleh, H., McGregor, N. E., Poulton, I. J., Scott, J. W., Gillespie, M. T., Kemp, B. E., and van Denderen, B. J. (2010) Germline deletion of AMP-activated protein kinase β subunits reduces bone mass without altering osteoclast differentiation or function. FASEBJ. 24, 275-285
15. Molinuevo, M. S., Schurman, L., McCarthy, A. D., Cortizo, A. M., Tolosa, M. J., Gangoiti, M. V., Arnol, V., and Sedlinsky, C. (2010) Effect of metformin on bone marrow progenitor cell differentiation. In vivo and in vitro studies. J. Bone Miner. Res. 25, 211-221
16. Shah, M., Kola, B., Bataveljic, A., Arnett, T. R., Viollet, B., Saxon, L., Korbonits, M., and Chenu, C. (2010) AMP-activated protein kinase (AMPK) activation regulates in vitro bone formation and bone mass. Bone 47, 309-319
17. Kim, J. E., Ahn, M. W., Baek, S. H., Lee, I. K., Kim, Y. W., Kim, J. Y., Dan, J. M., and Park, S. Y. (2008) AMPK activator, AICAR, inhibits palmitateinduced apoptosis in osteoblast. Bone 43, 394-404
18. Yamaguchi, N., Kukita, T., Li, Y. J., Kamio, N., Fukumoto, S., Nonaka, K., Ninomiya, Y., Hanazawa, S., and Yamashita, Y. (2008) Adiponectin inhibits induction of TNF-a/RANKL-stimulated NFATc1 via the AMPK signaling. FEBS Lett. 582, 451-456
19. Lee, S. H., Kim, B. J., Choi, H. J., Cho, S. W., Shin, C. S., Park, S. Y., Lee, Y. S., Lee, S. Y., Kim, H. H., Kim, G. S., and Koh, J. M. (2012) (-)-Epigallocathechin-3-gallate, an AMPK activator, decreases ovariectomy-induced bone loss by suppression of bone resorption. Calcif Tissue Int. 90, 404-410
20. Lee, Y. S., Kim, Y. S., Lee, S. Y., Kim, G. H., Kim, B. J., Lee, S. H., Lee, K. U., Kim, G. S., Kim, S. W., and Koh, J. M. (2010) AMP kinase acts as a negative regulator of RANKL in the differentiation of osteoclasts. Bone 47, 926-937
21. Li, Z., Jiang, H., Xie, W., Zhang, Z., Smrcka, A. V., and Wu, D. (2000) Roles of PLC-β2 and -β3 and PI3K7in chemoattractant-mediated signal transduction. Science 287, 1046-1049
22. Viollet, B., Andreelli, F., Jørgensen, S. B., Perrin, C., Geloen, A., Flamez, D., Mu, J., Lenzner, C., Baud, O., Bennoun, M., Gomas, E., Nicolas, G., Wojtaszewski, J. F., Kahn, A., Carling, D., Schuit, F. C., Birnbaum, M. J., Richter, E. A., Burcelin, R., and Vaulont, S. (2003) The AMP-activated protein kinase a2 catalytic subunit controls whole-body insulin sensitivity. J. Clin. Invest. 111, 91-98
23. Yokota, T., Kawakami, Y., Nagai, Y., Ma, J. X., Tsai, J. Y., Kincade, P. W., and Sato, S. (2006) Bone marrow lacks a transplantable progenitor for smooth muscle type α-actin-expressing cells. Stem Cells 24, 13-22
24. Khaliulin, I., Clarke, S. J., Lin, H., Parker, J., Suleiman, M. S., and Halestrap, A. P. (2007) Temperature preconditioning of isolated rat hearts. A potent cardioprotective mechanism involving a reduction in oxidative stress and inhibition of the mitochondrial permeability transition pore. J. Physiol. 581, 1147-1161
25. Liu, F., Lee, S. K., Adams, D. J., Gronowicz, G. A., and Kream, B. E. (2007) CREM deficiency in mice alters the response of bone to intermittent parathyroid hormone treatment. Bone 40, 1135-1143
26. Merrell, G. A., Troiano, N. W., Coady, C. E., and Kacena, M. A. (2005) Effects of long-term fixation on histological quality of undecalcified murine bones embedded in methylmethacrylate. Biotech. Histochem. 80, 139-146
27. Parfitt, A. M, Drezner, M. K., Glorieux, F. H., Kanis, J. A., Malluche, H., Meunier, P. J., Ott, S. M., and Recker, R. R. (1987) Bone histomorphometry. Standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 2, 595-610
28. Suda, T., Jimi, E., Nakamura, I., and Takahashi, N. (1997) Role of 1 a, 25-dihydroxyvitamin D3 in osteoclast differentiation and function. Methods Enzymol. 282, 223-235
29. Burgess, A. W., Metcalf, D., Kozka, I. J., Simpson, R. J., Vairo, G., Hamilton, J. A., and Nice, E. C. (1985) Purification of two forms of colony-stimulating factor from mouse L-cell-conditioned medium. J. Biol. Chem. 260, 16004-16011
30. Marshall, O. J. (2004) PerlPrimer. Cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20, 2471-2472
31. Schefe, J. H., Lehmann, K. E., Buschmann, I. R., Unger, T., and Funke-Kaiser, H. (2006) Quantitative real-time RT-PCR data analysis. Current concepts and the novel "gene expression's CT difference" formula. J. Mol. Med. 84, 901-910
32. Babij, P., Zhao, W., Small, C., Kharode, Y., Yaworsky, P. J., Bouxsein, M. L., Reddy, P. S., Bodine, P. V., Robinson, J. A., Bhat, B., Marzolf, J., Moran, R. A., and Bex, F. (2003) High bone mass in mice expressing a mutant LRP5 gene. J. Bone Miner. Res. 18, 960-974
33. Jeyabalan, J., Shah, M., Viollet, B., Roux, J. P., Chavassieux, P., Korbonits, M., and Chenu, C (2012) Mice lacking AMP-activated protein kinase a1 catalytic subunit have increased bone remodelling and modified skeletal responses to hormonal challenges induced by ovariectomy and intermittent PTH treatment. J. Endocrinol. 214, 349-358
34. Yagi, M., Miyamoto, T., Sawatani, Y., Iwamoto, K., Hosogane, N., Fujita, N., Morita, K., Ninomiya, K., Suzuki, T., Miyamoto, K., Oike, Y., Takeya, M., Toyama, Y., and Suda, T. (2005) DC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells. J. Exp. Med. 202, 345-351
35. Lee, S. H., Rho, J., Jeong, D., Sul, J. Y., Kim, T., Kim, N., Kang, J. S., Miyamoto, T., Suda, T., Lee, S. K., Pignolo, R. J., Koczon-Jaremko, B., Lorenzo, J., and Choi, Y. (2006) v-ATPase V0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat. Med. 12, 1403-1409
36. Cacicedo, J. M., Yagihashi, N., Keaney, J. F., Jr., Ruderman, N. B., and Ido, Y. (2004) AMPK inhibits fatty acid-induced increases in NF-kB transactivation in cultured human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 324, 1204-1209
37. Giri, S., Nath, N., Smith, B., Viollet, B., Singh, A. K., and Singh, I. (2004) 5-aminoimidazole-4-carboxamide-1-β-4-ribofuranoside inhibits proinflammatory response in glial cells. A possible role of AMP-activated protein kinase. J. Neurosci. 24, 479-487
38. Hattori, Y., Suzuki, K., Hattori, S., and Kasai, K. (2006) Metformin inhibits cytokine-induced nuclear factor αB activation via AMP-activated protein kinase activation in vascular endothelial cells. Hypertension 47, 1183-1188
39. Yang, Z., Kahn, B. B., Shi, H., and Xue, B. Z. (2010) Macrophage a1 AMP-activated protein kinase (a1AMPK) antagonizes fatty acid-induced inflammation through SIRT1. J. Biol. Chem. 285, 19051-19059
40. Bess, E., Fisslthaler, B., Frömel, T., and Fleming, I. (2011) Nitric oxideinduced activation of the AMP-activated protein kinase a2 subunit attenuates IkB kinase activity and inflammatory responses in endothelial cells. PLoS One 6, e20848
41. Katerelos, M., Mudge, S. J., Stapleton, D., Auwardt, R. B., Fraser, S. A., Chen, C. G., Kemp, B. E., and Power, D. A. (2010) 5-Aminoimidazole-4- carboxamide ribonucleoside and AMP-activated protein kinase inhibit signalling through NF-kB. Immunol Cell Biol. 88, 754-760
42. Pearce, E. L., Walsh, M. C., Cejas, P. J., Harms, G. M., Shen, H., Wang, L. S., Jones, R. G., and Choi, Y. (2009) Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 460, 103-107
43. Galic, S., Fullerton, M. D., Schertzer, J. D., Sikkema, S., Marcinko, K., Walkley, C. R., Izon, D., Honeyman, J., Chen, Z. P., van Denderen, B. J., Kemp, B. E., and Steinberg, G. R. (2011) Hematopoietic AMPK β1 reduces mouse adipose tissue macrophage inflammation and insulin resistance in obesity. J. Clin. Invest. 121, 4903-4915
44. Tanaka, Y. (2005) [Inflammatory cytokines for osteoclastogenesis]. Nihon Rinsho 63, 1535-1540
45. Mao, J., Yang, T., Gu, Z., Heird, W. C., Finegold, M. J., Lee, B., and Wakil, S. J. (2009) aP2-Cre-mediated inactivation of acetyl-CoA carboxylase 1 causes growth retardation and reduced lipid accumulation in adipose tissues. Proc. Natl. Acad. Sci. U. S. A. 106, 17576-17581
46. Ha, J., Daniel, S., Broyles, S. S., and Kim, K. H. (1994) Critical phosphorylation sites for acetyl-CoA carboxylase activity. J. Biol. Chem. 269, 22162-22168
47. Zhang, B. B., Zhou, G., and Li, C. (2009) AMPK. An emerging drug target for diabetes and the metabolic syndrome. Cell Metab. 9, 407-416
48. Reznick, R. M., Zong, H., Li, J., Morino, K., Moore, I. K., Yu, H. J., Liu, Z. X., Dong, J., Mustard, K. J., Hawley, S. A., Befroy, D., Pypaert, M., Hardie, D. G., Young, L. H., and Shulman, G. I. (2007) Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab. 5, 151-156