Differential roles of MAPK kinases MKK3 and MKK6 in osteoclastogenesis and bone loss

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Boyle, David L ^a   Hammaker, Deepa ^a   Edgar, Meghan ^a   Zaiss, Mario M ^b   Teufel, Stefan ^c   David, Jean Pierre ^c   Schett, Georg ^d   Firestein, Gary S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EPFL   (Switzerland)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN K; ESTROGEN; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 6; TRANSCRIPTION FACTOR NFATC1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL COUNT; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME INHIBITION; ENZYME REGULATION; ESTROGEN DEFICIENCY; FEMALE; IN VITRO STUDY; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; OVARIECTOMY-INDUCED OSTEOPOROSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; BONE AND BONES; BONE RESORPTION; FEMALE; GENE EXPRESSION; MAP KINASE KINASE 3; MAP KINASE KINASE 6; MICE; MICE, KNOCKOUT; OSTEOCLASTS; OVARIECTOMY;

EID: 84896483549     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084818     Document Type: Article

References (44)

1. Khosla S (2001) Minireview: the OPG/RANKL/RANK system. Endocrinology 142: 5050-5055.
2. Kimble RB, Srivastava S, Ross FP, Matayoshi A, Pacifici R (1996) Estrogen deficiency increases the ability of stromal cells to support murine osteoclastogenesis via an interleukin-1and tumor necrosis factor-mediated stimulation of macrophage colony-stimulating factor production. J Biol Chem 271: 28890-28897. (Pubitemid 26382589)
3. Manolagas SC (1995) Role of cytokines in bone resorption. Bone 17: 63S-67S.
4. Wei S, Kitaura H, Zhou P, Ross FP, Teitelbaum SL (2005) IL-1 mediates TNF-induced osteoclastogenesis. J Clin Invest 115: 282-290. (Pubitemid 40385470)
5. Kim JH, Jin HM, Kim K, Song I, Youn BU, et al. (2009) The mechanism of osteoclast differentiation induced by IL-1. J Immunol 183: 1862-1870.
6. Faienza MF, Ventura A, Marzano F, Cavallo L (2013) Postmenopausal osteoporosis: the role of immune system cells. Clin Dev Immunol 2013: 575936.
7. David JP, Schett G (2010) TNF and bone. Curr Dir Autoimmun 11: 135-144.
8. Feng X (2005) RANKing intracellular signaling in osteoclasts. IUBMB Life 57: 389-395.
9. Raggatt LJ, Partridge NC (2010) Cellular and molecular mechanisms of bone remodeling. J Biol Chem 285: 25103-25108.
10. Boyle WJ, Simonet WS, Lacey DL (2003) Osteoclast differentiation and activation. Nature 423: 337-342. (Pubitemid 40852708)
11. Asagiri M, Takayanagi H (2007) The molecular understanding of osteoclast differentiation. Bone 40: 251-264. (Pubitemid 46054562)
12. Strait K, Li Y, Dillehay DL, Weitzmann MN (2008) Suppression of NF-kappaB activation blocks osteoclastic bone resorption during estrogen deficiency. Int J Mol Med 21: 521-525. (Pubitemid 351802648)
13. Zwerina J, Hayer S, Redlich K, Bobacz K, Kollias G, et al. (2006) Activation of p38 MAPK is a key step in tumor necrosis factor-mediated inflammatory bone destruction. Arthritis Rheum 54: 463-472. (Pubitemid 43228620)
14. Sharma SM, Bronisz A, Hu R, Patel K, Mansky KC, et al. (2007) MITF and PU.1 recruit p38 MAPK and NFATc1 to target genes during osteoclast differentiation. J Biol Chem 282: 15921-15929. (Pubitemid 47093311)
15. Troen BR (2006) The regulation of cathepsin K gene expression. Ann N Y Acad Sci 1068: 165-172.
16. Bohm C, Hayer S, Kilian A, Zaiss MM, Finger S, et al. (2009) The alpha-isoform of p38 MAPK specifically regulates arthritic bone loss. J Immunol 183: 5938-5947.
17. Hill RJ, Dabbagh K, Phippard D, Li C, Suttmann RT, et al. (2008) Pamapimod, a novel p38 mitogen-activated protein kinase inhibitor: preclinical analysis of efficacy and selectivity. J Pharmacol Exp Ther 327: 610-619.
18. Caverzasio J, Higgins L, Ammann P (2008) Prevention of trabecular bone loss induced by estrogen deficiency by a selective aaalpha inhibitor. J Bone Miner Res 23: 1389-1397.
19. Medicherla S, Ma JY, Mangadu R, Jiang Y, Zhao JJ, et al. (2006) A selective p38 alpha mitogen-activated protein kinase inhibitor reverses cartilage and bone destruction in mice with collagen-induced arthritis. J Pharmacol Exp Ther 318: 132-141.
20. Inoue T, Hammaker D, Boyle DL, Firestein GS (2005) Regulation of p38 MAPK by MAPK kinases 3 and 6 in fibroblast-like synoviocytes. J Immunol 174: 4301-4306. (Pubitemid 40396012)
21. Yoshizawa T, Hammaker D, Boyle DL, Corr M, Flavell R, et al. (2009) Role of MAPK kinase 6 in arthritis: distinct mechanism of action in inflammation and cytokine expression. J Immunol 183: 1360-1367.
22. Hammaker D, Topolewski K, Edgar M, Yoshizawa T, Fukushima A, et al. (2012) Decreased collagen-induced arthritis severity and adaptive immunity in MKK-6-deficient mice. Arthritis Rheum 64: 678-687.
23. Inoue T, Boyle DL, Corr M, Hammaker D, Davis RJ, et al. (2006) Mitogen-activated protein kinase kinase 3 is a pivotal pathway regulating p38 activation in inflammatory arthritis. Proc Natl Acad Sci U S A 103: 5484-5489.
24. Boyle DL, Rosengren S, Bugbee W, Kavanaugh A, Firestein GS (2003) Quantitative biomarker analysis of synovial gene expression by real-time PCR. Arthritis Res Ther 5: R352-360.
25. Matsumoto M, Sudo T, Saito T, Osada H, Tsujimoto M (2000) Involvement of p38 mitogen-activated protein kinase signaling pathway in osteoclastogenesis mediated by receptor activator of NF-kappa B ligand (RANKL). J Biol Chem 275: 31155-31161.
26. Mbalaviele G, Anderson G, Jones A, De Ciechi P, Settle S, et al. (2006) Inhibition of p38 mitogen-activated protein kinase prevents inflammatory bone destruction. J Pharmacol Exp Ther 317: 1044-1053. (Pubitemid 43764107)
27. Matsumoto M, Sudo T, Maruyama M, Osada H, Tsujimoto M (2000) Activation of p38 mitogen-activated protein kinase is crucial in osteoclastogenesis induced by tumor necrosis factor. Febs Lett 486: 23-28.
28. Huang H, Chang EJ, Ryu J, Lee ZH, Lee Y, et al. (2006) Induction of c-Fos and NFATc1 during RANKL-stimulated osteoclast differentiation is mediated by the p38 signaling pathway. Biochem Biophys Res Commun 351: 99-105. (Pubitemid 44635412)
29. So H, Rho J, Jeong D, Park R, Fisher DE, et al. (2003) Microphthalmia transcription factor and PU.1 synergistically induce the leukocyte receptor osteoclast-associated receptor gene expression. J Biol Chem 278: 24209-24216. (Pubitemid 36830257)
30. Sundaram K, Nishimura R, Senn J, Youssef RF, London SD, et al. (2007) RANK ligand signaling modulates the matrix metalloproteinase-9 gene expression during osteoclast differentiation. Exp Cell Res 313: 168-178. (Pubitemid 44958461)
31. Yamashita T, Kobayashi Y, Mizoguchi T, Yamaki M, Miura T, et al. (2008) MKK6-p38 MAPK signaling pathway enhances survival but not bone-resorbing activity of osteoclasts. Biochem Biophys Res Commun 365: 252-257. (Pubitemid 350137282)
32. Huang H, Ryu J, Ha J, Chang EJ, Kim HJ, et al. (2006) Osteoclast differentiation requires TAK1 and MKK6 for NFATc1 induction and NF-kappaB transactivation by RANKL. Cell Death Differ 13: 1879-1891. (Pubitemid 44542401)
33. Khosla S, Oursler MJ, Monroe DG (2012) Estrogen and the skeleton. Trends Endocrinol Metab 23: 576-581.
34. Armas LA, Recker RR (2012) Pathophysiology of osteoporosis: new mechanistic insights. Endocrinol Metab Clin North Am 41: 475-486.
35. Shibata T, Shira-Ishi A, Sato T, Masaki T, Masuda A, et al. (2002) Vitamin D hormone inhibits osteoclastogenesis in vivo by decreasing the pool of osteoclast precursors in bone marrow. J Bone Miner Res 17: 622-629. (Pubitemid 34246637)
36. Bolon B, Carter C, Daris M, Morony S, Capparelli C, et al. (2001) Adenoviral delivery of osteoprotegerin ameliorates bone resorption in a mouse ovariectomy model of osteoporosis. Mol Ther 3: 197-205. (Pubitemid 32509822)
37. Krum SA, Brown M (2008) Unraveling estrogen action in osteoporosis. Cell Cycle 7: 1348-1352. (Pubitemid 351872572)
38. Krum SA, Miranda-Carboni GA, Hauschka PV, Carroll JS, Lane TF, et al. (2008) Estrogen protects bone by inducing Fas ligand in osteoblasts to regulate osteoclast survival. EMBO J 27: 535-545. (Pubitemid 351225684)
39. Nakamura T, Imai Y, Matsumoto T, Sato S, Takeuchi K, et al. (2007) Estrogen prevents bone loss via estrogen receptor alpha and induction of Fas ligand in osteoclasts. Cell 130: 811-823. (Pubitemid 47332572)
40. Passeri G, Girasole G, Jilka RL, Manolagas SC (1993) Increased interleukin-6 production by murine bone marrow and bone cells after estrogen withdrawal. Endocrinology 133: 822-828. (Pubitemid 23238898)
41. Srivastava S, Weitzmann MN, Kimble RB, Rizzo M, Zahner M, et al. (1998) Estrogen blocks M-CSF gene expression and osteoclast formation by regulating phosphorylation of Egr-1 and its interaction with Sp-1. J Clin Invest 102: 1850-1859. (Pubitemid 28533832)
42. Tyagi AM, Srivastava K, Mansoori MN, Trivedi R, Chattopadhyay N, et al. (2012) Estrogen deficiency induces the differentiation of IL-17 secreting Th17 cells: a new candidate in the pathogenesis of osteoporosis. PLoS One 7: e44552.
43. Tokuda H, Kanno Y, Ishisaki A, Takenaka M, Harada A, et al. (2004) Interleukin (IL)-17 enhances tumor necrosis factor-alpha-stimulated IL-6 synthesis via p38 mitogen-activated protein kinase in osteoblasts. J Cell Biochem 91: 1053-1061.
44. Greenblatt MB, Shim JH, Zou W, Sitara D, Schweitzer M, et al. (2010) The p38 MAPK pathway is essential for skeletogenesis and bone homeostasis in mice. J Clin Invest 120: 2457-2473.