The p38α MAPK function in osteoprecursors is required for bone formation and bone homeostasis in adult mice

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Rodríguez Carballo, Edgardo ^a   Gámez, Beatriz ^a   Sedó Cabezón, Lara ^a   Sánchez Feutrie, Manuela ^a,b,c   Zorzano, Antonio ^a,b,c   Manzanares Céspedes, Cristina ^a   Rosa, José Luis ^a   Ventura, Francesc ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ALPHA TUBULIN; CRE RECOMBINASE; DOXYCYCLINE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 14; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE ANABOLISM; BONE CHARACTERISTICS AND FUNCTIONS; BONE DEVELOPMENT; BONE HOMEOSTASIS; BONE MARROW CELL; BONE MASS; BONE MINERALIZATION; BONE REMODELING; CALVARIA; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CONTROLLED STUDY; CORTICAL BONE; ENCHONDRAL OSSIFICATION; ENZYME ACTIVITY; FEMUR; GENE DELETION; KNOCKOUT MOUSE; LONG BONE; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; TRABECULAR BONE; ABNORMALITIES; ANIMAL; ANTIBODY SPECIFICITY; EMBRYOLOGY; GENE INACTIVATION; GENETICS; HOMEOSTASIS; METABOLISM; NEWBORN; SKULL;

ANIMALS; ANIMALS, NEWBORN; FEMUR; GENE KNOCKOUT TECHNIQUES; HOMEOSTASIS; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 14; ORGAN SPECIFICITY; OSTEOBLASTS; OSTEOGENESIS; SKULL;

EID: 84904092797     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102032     Document Type: Article

References (54)

1. Raggatt LJ, Partridge NC (2010) Cellular and molecular mechanisms of bone remodeling. J Biol Chem 285: 25103-25108.
2. Karsenty G (2008) Transcriptional control of skeletogenesis. Annu Rev Genomics Hum Genet 9: 183-196.
3. Karsenty G, Kronenberg HM, Settembre C (2009) Genetic control of bone formation. Annu Rev Cell Dev Biol 25: 629-648.
4. Zaidi M (2007) Skeletal remodeling in health and disease. Nat Med 13: 791-801.
5. Greenblatt MB, Shim JH, Glimcher LH (2013) Mitogen-Activated Protein Kinase Pathways in Osteoblasts. Annu Rev Cell Dev Biol.
6. Cuadrado A, Nebreda AR (2010) Mechanisms and functions of p38 MAPK signalling. Biochem J 429: 403-417.
7. 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.
8. Guicheux J, Lemonnier J, Ghayor C, Suzuki A, Palmer G, et al. (2003) Activation of p38 mitogen-activated protein kinase and c-Jun-NH2-terminal kinase by BMP-2 and their implication in the stimulation of osteoblastic cell differentiation. J Bone Miner Res 18: 2060-2068. (Pubitemid 37377457)
9. Vinals F, Lopez-Rovira T, Rosa JL, Ventura F (2002) Inhibition of PI3K/p70 S6K and p38 MAPK cascades increases osteoblastic differentiation induced by BMP-2. FEBS Lett 510: 99-104. (Pubitemid 34084891)
10. Caverzasio J, Higgins L, Ammann P (2008) Prevention of trabecular bone loss induced by estrogen deficiency by a selective p38alpha inhibitor. J Bone Miner Res 23: 1389-1397.
11. Celil AB, Hollinger JO, Campbell PG (2005) Osx transcriptional regulation is mediated by additional pathways to BMP2/Smad signaling. J Cell Biochem 95: 518-528. (Pubitemid 41420182)
12. Wang X, Goh CH, Li B (2007) p38 mitogen-activated protein kinase regulates osteoblast differentiation through osterix. Endocrinology 148: 1629-1637. (Pubitemid 46457114)
13. Ulsamer A, Ortuno MJ, Ruiz S, Susperregui AR, Osses N, et al. (2008) BMP-2 induces Osterix expression through up-regulation of Dlx5 and its phosphorylation by p38. J Biol Chem 283: 3816-3826.
14. Ortuno MJ, Ruiz-Gaspa S, Rodriguez-Carballo E, Susperregui AR, Bartrons R, et al. (2010) p38 regulates expression of osteoblast-specific genes by phosphorylation of osterix. J Biol Chem 285: 31985-31994.
15. Ortuno MJ, Susperregui AR, Artigas N, Rosa JL, Ventura F (2013) Osterix induces Col1a1 gene expression through binding to Sp1 sites in the bone enhancer and proximal promoter regions. Bone 52: 548-556.
16. Ge C, Yang Q, Zhao G, Yu H, Kirkwood KL, et al. (2012) Interactions between extracellular signal-regulated kinase 1/2 and p38 MAP kinase pathways in the control of RUNX2 phosphorylation and transcriptional activity. J Bone Miner Res 27: 538-551.
17. Sinha KM, Yasuda H, Coombes MM, Dent SY, de Crombrugghe B (2010) Regulation of the osteoblast-specific transcription factor Osterix by NO66, a Jumonji family histone demethylase. EMBO J 29: 68-79.
18. Thouverey C, Caverzasio J (2012) The p38alpha MAPK positively regulates osteoblast function and postnatal bone acquisition. Cell Mol Life Sci 69: 3115-3125.
19. Rodda SJ, McMahon AP (2006) Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133: 3231-3244. (Pubitemid 44404346)
20. Davey RA, Clarke MV, Sastra S, Skinner JP, Chiang C, et al. (2012) Decreased body weight in young Osterix-Cre transgenic mice results in delayed cortical bone expansion and accrual. Transgenic Res 21: 885-893.
21. Salazar VS, Zarkadis N, Huang L, Norris J, Grimston SK, et al. (2013) Embryonic ablation of osteoblast Smad4 interrupts matrix synthesis in response to canonical Wnt signaling and causes an osteogenesis-imperfecta-like phenotype. J Cell Sci 126: 4974-4984.
22. Dacic S, Kalajzic I, Visnjic D, Lichtler AC, Rowe DW (2001) Col1a1-driven transgenic markers of osteoblast lineage progression. J Bone Miner Res 16: 1228-1236. (Pubitemid 32574651)
23. Bonewald LF (2011) The amazing osteocyte. J Bone Miner Res 26: 229-238.
24. Matsubara T, Kida K, Yamaguchi A, Hata K, Ichida F, et al. (2008) BMP2 regulates Osterix through Msx2 and Runx2 during osteoblast differentiation. J Biol Chem 283: 29119-29125.
25. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, et al. (2002) The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108: 17-29. (Pubitemid 34137009)
26. Seibel MJ (2005) Biochemical markers of bone turnover: part I: biochemistry and variability. Clin Biochem Rev 26: 97-122.
27. Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Boyle WJ, et al. (2000) The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption. J Bone Miner Res 15: 2-12. (Pubitemid 30026926)
28. Hanson DA, Weis MA, Bollen AM, Maslan SL, Singer FR, et al. (1992) A specific immunoassay for monitoring human bone resorption: quantitation of type I collagen cross-linked N-telopeptides in urine. J Bone Miner Res 7: 1251-1258. (Pubitemid 23000964)
29. Glatt V, Canalis E, Stadmeyer L, Bouxsein ML (2007) Age-related changes in trabecular architecture differ in female and male C57BL/6J mice. J Bone Miner Res 22: 1197-1207. (Pubitemid 351339702)
30. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, et al. (2010) Guidelines for assessment of bone microstructure in rodents using microcomputed tomography. J Bone Miner Res 25: 1468-1486.
31. Ferguson VL, Ayers RA, Bateman TA, Simske SJ (2003) Bone development and age-related bone loss in male C57BL/6J mice. Bone 33: 387-398. (Pubitemid 37107464)
32. Price C, Herman BC, Lufkin T, Goldman HM, Jepsen KJ (2005) Genetic variation in bone growth patterns defines adult mouse bone fragility. J Bone Miner Res 20: 1983-1991. (Pubitemid 41532784)
33. Bidder M, Latifi T, Towler DA (1998) Reciprocal temporospatial patterns of Msx2 and Osteocalcin gene expression during murine odontogenesis. J Bone Miner Res 13: 609-619. (Pubitemid 28163012)
34. Miller LM, Little W, Schirmer A, Sheik F, Busa B, et al. (2007) Accretion of bone quantity and quality in the developing mouse skeleton. J Bone Miner Res 22: 1037-1045. (Pubitemid 351339726)
35. Maatta JA, Buki KG, Gu G, Alanne MH, Vaaraniemi J, et al. (2013) Inactivation of estrogen receptor alpha in bone-forming cells induces bone loss in female mice. FASEB J 27: 478-488.
36. Fritton JC, Myers ER, Wright TM, van der Meulen MC (2008) Bone mass is preserved and cancellous architecture altered due to cyclic loading of the mouse tibia after orchidectomy. J Bone Miner Res 23: 663-671. (Pubitemid 351575020)
37. Hamrick MW, Ding KH, Ponnala S, Ferrari SL, Isales CM (2008) Caloric restriction decreases cortical bone mass but spares trabecular bone in the mouse skeleton: implications for the regulation of bone mass by body weight. J Bone Miner Res 23: 870-878. (Pubitemid 351768805)
38. Seeman E (2001) Unresolved issues in osteoporosis in men. Rev Endocr Metab Disord 2: 45-64.
39. Frost HM (1999) On the trabecular "thickness"-number problem. J Bone Miner Res 14: 1816-1821.
40. Hamrick MW, Ferrari SL (2008) Leptin and the sympathetic connection of fat to bone. Osteoporos Int 19: 905-912. (Pubitemid 351758616)
41. Anand P, Shenoy R, Palmer JE, Baines AJ, Lai RY, et al. (2011) Clinical trial of the p38 MAP kinase inhibitor dilmapimod in neuropathic pain following nerve injury. Eur J Pain 15: 1040-1048.
42. Joos H, Albrecht W, Laufer S, Brenner RE (2010) Differential effects of p38MAP kinase inhibitors on the expression of inflammation-associated genes in primary, interleukin-1beta-stimulated human chondrocytes. Br J Pharmacol 160: 1252-1262.
43. Wagner EF, Nebreda AR (2009) Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9: 537-549.
44. Payne KA, Meszaros LB, Phillippi JA, Huard J (2010) Effect of phosphatidyl inositol 3-kinase, extracellular signal-regulated kinases 1/2, and p38 mitogen-activated protein kinase inhibition on osteogenic differentiation of muscle-derived stem cells. Tissue Eng Part A 16: 3647-3655.
45. Gamell C, Susperregui AG, Bernard O, Rosa JL, Ventura F (2011) The p38/MK2/Hsp25 pathway is required for BMP-2-induced cell migration. PLoS One 6: e16477.
46. Kawano T, Zhu M, Troiano N, Horowitz M, Bian J, et al. (2013) LIM kinase 1 deficient mice have reduced bone mass. Bone 52: 70-82.
47. Zhou FH, Foster BK, Zhou XF, Cowin AJ, Xian CJ (2006) TNF-alpha mediates p38 MAP kinase activation and negatively regulates bone formation at the injured growth plate in rats. J Bone Miner Res 21: 1075-1088. (Pubitemid 43962836)
48. Beardmore VA, Hinton HJ, Eftychi C, Apostolaki M, Armaka M, et al. (2005) Generation and characterization of p38beta (MAPK11) gene-targeted mice. Mol Cell Biol 25: 10454-10464. (Pubitemid 41681967)
49. Cuenda A, Rousseau S (2007) p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim Biophys Acta 1773: 1358-1375. (Pubitemid 47125981)
50. Zhang C, Cho K, Huang Y, Lyons JP, Zhou X, et al. (2008) Inhibition of Wnt signaling by the osteoblast-specific transcription factor Osterix. Proc Natl Acad Sci U S A 105: 6936-6941. (Pubitemid 351754508)
51. Koga T, Matsui Y, Asagiri M, Kodama T, de Crombrugghe B, et al. (2005) NFAT and Osterix cooperatively regulate bone formation. Nat Med 11: 880-885. (Pubitemid 41161121)
52. Gamez B, Rodriguez-Carballo E, Bartrons R, Rosa JL, Ventura F (2013) MicroRNA-322 (miR-322) and its target protein Tob2 modulate Osterix (Osx) mRNA stability. J Biol Chem 288: 14264-14275.
53. Zhou X, Zhang Z, Feng JQ, Dusevich VM, Sinha K, et al. (2010) Multiple functions of Osterix are required for bone growth and homeostasis in postnatal mice. Proc Natl Acad Sci U S A 107: 12919-12924.
54. Heinrichsdorff J, Luedde T, Perdiguero E, Nebreda AR, Pasparakis M (2008) p38 alpha MAPK inhibits JNK activation and collaborates with IkappaB kinase 2 to prevent endotoxin-induced liver failure. EMBO Rep 9: 1048-1054.