Decreased oxidative stress and greater bone anabolism in the aged, when compared to the young, murine skeleton with parathyroid hormone administration

Aging Cell

Volumn 9, Issue 5, 2010, Pages 851-867

  Jilka, Robert L ^a   Almeida, Maria ^a   Ambrogini, Elena ^a   Han, Li ^a   Roberson, Paula K ^a   Weinstein, Robert S ^a   Manolagas, Starros C ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Bone formation; Osteoblasts; Osteoporosis; Oxidative stress; Parathyroid hormone

Indexed keywords

ACETYLCYSTEINE; CATALASE; FORKHEAD TRANSCRIPTION FACTOR; GLUTATHIONE; LIPOXYGENASE; PARATHYROID HORMONE; PROTEIN P66; REACTIVE OXYGEN METABOLITE; WNT PROTEIN;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE AGE; BONE DENSITY; BONE MASS; BONE METABOLISM; BONE REMODELING; BONE STRENGTH; CALVARIA; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVITY; FEMALE; FEMUR; HUMAN; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOLYSIS; OUTCOME ASSESSMENT; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRABECULAR BONE;

AGING; ANIMALS; ANTIOXIDANTS; APOPTOSIS; ARACHIDONATE 12-LIPOXYGENASE; ARACHIDONATE 15-LIPOXYGENASE; BONE AND BONES; BONE DENSITY; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; MICE; MICE, INBRED C57BL; MULTIENZYME COMPLEXES; OSTEOBLASTS; OXIDATIVE STRESS; PARATHYROID HORMONE; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; WNT PROTEINS;

MURINAE; MUS;

EID: 78349266526     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2010.00616.x     Document Type: Article

References (69)

1. Abou-Samra AB, Jüppner H, Force T, Freeman MW, Kong XF, Schipani E, Urena P, Richards J, Bonventre JV, Potts JT, Kronenberg HM, Segre GV (1992) Expression cloning of a common receptor for parathyroid hormone and parathyroid hormone-related peptide from rat osteoblast-like cells: a single receptor stimulates intracellular accumulation of both cAMP and inositol trisphosphates and increases intracellular free calcium. Proc. Natl Acad. Sci. USA 89, 2732-2736.
2. Almeida M, Han L, Bellido T, Manolagas SC, Kousteni S (2005) Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by β-catenin-dependent and independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT. J. Biol. Chem. 280, 41342-41351.
3. Almeida M, Han L, Martin-Millan M, O'Brien CA, Manolagas SC (2007a) Oxidative stress antagonizes Wnt signaling in osteoblast precursors by diverting β-catenin from T cell factor- to Forkhead box O-mediated transcription. J. Biol. Chem. 282, 27298-27305.
4. Almeida M, Han L, Martin-Millan M, Plotkin LI, Stewart SA, Roberson PK, Kousteni S, O'Brien CA, Bellido T, Parfitt AM, Weinstein RS, Jilka RL, Manolagas SC (2007b) Skeletal involution and oxidative stress: effects of aging accelerated by loss of sex steroids. J. Biol. Chem. 282, 27285-27297.
5. Almeida M, Ambrogini E, Martin-Millan M, Han L, Warren A, Shelton R, Plotkin L, Bellido T, O'Brien CA, Jilka RL, Weinstein RS, Manolagas SC (2008) Induction of oxidative stress and diversion of β-catenin from TCF- to FOXO-mediated transcription by glucocorticoids or TNFα in osteoblastic cells. J. Bone Miner. Res. 23, S170.
6. Almeida M, Ambrogini E, Han L, Manolagas SC, Jilka RL (2009) Increased lipid oxidation causes oxidative stress, increased PPARγ expression and diminished pro-osteogenic Wnt signaling in the skeleton. J. Biol. Chem. 284, 27438-27448.
7. shc siganaling cascade: counter regulation by estrogens or androgens. Mol. Endocrinol., in press, doi:.
8. Ambrogini E, Almeida M, Martin-Millan M, Paik JH, DePinho RA, Han L, Goellner J, Weinstein RS, Jilka RL, O'Brien CA, Manolagas SC (2010) FoxO-Mediated defense against oxidative stress in osteoblasts is indispensable for skeletal homeostasis in mice. Cell Metab. 11, 136-146.
9. Bellido T, Ali AA, Plotkin LI, Fu Q, Gubrij I, Roberson PK, Weinstein RS, O'Brien CA, Manolagas SC, Jilka RL (2003) Proteasomal degradation of Runx2 shortens parathyroid hormone-induced anti-apoptotic signaling in osteoblasts: a putative explanation for why intermittent administration is needed for bone anabolism. J. Biol. Chem. 278, 50259-50272.
10. Bellido T, Ali AA, Gubrij I, Plotkin LI, Fu Q, O'Brien CA, Manolagas SC, Jilka RL (2005) Chronic elevation of parathyroid hormone in mice reduces expression of sclerostin by osteocytes: a novel mechanism for hormonal control of osteoblastogenesis. Endocrinology 146, 4577-4583.
11. Bodine PV (2008) Wnt signaling control of bone cell apoptosis. Cell Res. 18, 248-253.
12. Bodine PV, Seestaller-Wehr L, Kharode YP, Bex FJ, Komm BS (2007) Bone anabolic effects of parathyroid hormone are blunted by deletion of the Wnt antagonist secreted frizzled-related protein-1. J. Cell. Physiol. 210, 352-357.
13. Brennan TC, Rizzoli R, Ammann P (2009) Selective modification of bone quality by PTH, pamidronate, or raloxifene. J. Bone Miner. Res. 24, 800-808.
14. Chamorro MN, Schwartz DR, Vonica A, Brivanlou AH, Cho KR, Varmus HE (2005) FGF-20 and DKK1 are transcriptional targets of β-catenin and FGF-20 is implicated in cancer and development. EMBO J. 24, 73-84.
15. Chen C, Koh AJ, Datta NS, Zhang J, Keller ET, Xiao G, Franceschi RT, D'Silva NJ, McCauley LK (2004) Impact of the mitogen-activated protein kinase pathway on parathyroid hormone-related protein actions in osteoblasts. J. Biol. Chem. 279, 29121-29129.
16. Compston JE (2007) Skeletal actions of intermittent parathyroid hormone: effects on bone remodelling and structure. Bone 40, 1447-1452.
17. Di Gregorio GB, Yamamoto M, Ali AA, Abe E, Roberson P, Manolagas SC, Jilka RL (2001) Attenuation of the self-renewal of transit-amplifying osteoblast progenitors in the murine bone marrow by 17β-estradiol. J. Clin. Invest. 107, 803-812.
18. Funato Y, Michiue T, Asashima M, Miki H (2006) The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-beta-catenin signalling through dishevelled. Nat. Cell Biol. 8, 501-508.
19. Galli C, Fu Q, Wang W, Olsen BR, Manolagas SC, Jilka RL, O'Brien CA (2009) Commitment to the osteoblast lineage is not required for RANKL gene expression. J. Biol. Chem. 284, 12654-12662.
20. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, Pelliccia G, Luzi L, Minucci S, Marcaccio M, Pinton P, Rizzuto R, Bernardi P, Paolucci F, Pelicci PG (2005) Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122, 221-233.
21. Glass II DA, Bialek P, Ahn JD, Starbuck M, Patel MS, Clevers H, Taketo MM, Long F, McMahon AP, Lang RA, Karsenty G (2005) Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev. Cell 8, 751-764.
22. 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.
23. Guo J, Liu M, Yang D, Bouxsein ML, Saito H, Galvin S, Kuhstoss SA, Thomas CC, Schipani E, Baron R, Bringhurst FR, Kronenberg HM (2010a) Suppression of Wnt signaling by Dkk1 attenuates PTH-mediated stromal cell response and new bone formation. Cell Metab. 11, 161-171.
24. Guo J, Liu M, Yang D, Bouxsein ML, Thomas CC, Schipani E, Bringhurst FR, Kronenberg HM (2010b) Phospholipase C signaling via the parathyroid Hormone (PTH)/PTH-related peptide receptor is essential for normal bone responses to PTH. Endocrinology 151, 3502-3513.
25. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, Da Costa LT, Morin PJ, Vogelstein B, Kinzler KW (1998) Identification of c-MYC as a target of the APC pathway. Science 281, 1509-1512.
26. Van Der Heyden MA, Rook MB, Hermans MM, Rijksen G, Boonstra J, Defize LH, Destree OH (1998) Identification of connexin43 as a functional target for Wnt signalling. J. Cell Sci. 111, 1741-1749.
27. Hodsman AB, Bauer DC, Dempster D, Dian L, Hanley DA, Harris ST, Kendler D, McClung MR, Miller PD, Olszynski WP, Orwoll E, Yuen CK (2005) Parathyroid hormone and teriparatide for the treatment of osteoporosis: a review of the evidence and suggested guidelines for its use. Endocr. Rev. 26, 688-703.
28. Horowitz MC, Coleman DL, Flood PM, Kupper TS, Jilka RL (1989) Parathyroid hormone and lipopolysaccharide induce murine osteoblast-like cells to secrete a cytokine indistinguishable from granulocyte-macrophage colony-stimulating factor. J. Clin. Invest. 83, 149-157.
29. Jackson A, Vayssiere B, Garcia T, Newell W, Baron R, Roman-Roman S, Rawadi G (2005) Gene array analysis of Wnt-regulated genes in C3H10T1/2 cells. Bone 36, 585-598.
30. Janssen-Heininger YM, Mossman BT, Heintz NH, Forman HJ, Kalyanaraman B, Finkel T, Stamler JS, Rhee SG, Van Der Vliet A (2008) Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radic. Biol. Med. 45, 1-17.
31. Jia D, O'Brien CA, Stewart SA, Manolagas SC, Weinstein RS (2006) Glucocorticoids act directly on osteoclasts to increase their life span and reduce bone density. Endocrinology 147, 5592-5599.
32. Jilka RL (1986) Parathyroid hormone-stimulated development of osteoclasts in cultures of cells from neonatal murine calvaria. Bone 7, 29-40.
33. Jilka RL (2007) Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone 40, 1434-1446.
34. Jilka RL, Weinstein RS, Bellido T, Roberson P, Parfitt AM, Manolagas SC (1999) Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J. Clin. Invest. 104, 439-446.
35. Jilka RL, Weinstein RS, Parfitt AM, Manolagas SC (2007) Quantifying osteoblast and osteocyte apoptosis: challenges and rewards. J. Bone Miner. Res. 22, 1492-1501.
36. Jilka RL, O'Brien CA, Ali AA, Roberson PK, Weinstein RS, Manolagas SC (2009) Intermittent PTH stimulates periosteal bone formation by actions on post-mitotic preosteoblasts. Bone 44, 275-286.
37. Jilka RL, O'Brien CA, Weinstein RS, Manolagas SC (2010) Continuous elevation of PTH increases the number of osteoblasts via both osteoclast-dependent and- independent mechanisms. J. Bone Miner. Res., in press. doi:.
38. Keller H, Kneissel M (2005) SOST is a target gene for PTH in bone. Bone 37, 148-158.
39. Kleerekoper M, Villanueva AR, Stanciu J, Rao DS, Parfitt AM (1985) The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif. Tissue Int. 37, 594-597.
40. Knopp E, Troiano N, Bouxsein M, Sun Bh, Lostritto K, Gundberg C, Dziura J, Insogna K (2005) The effect of aging on the skeletal response to intermittent treatment with parathyroid hormone. Endocrinology 146, 1983-1990.
41. Kramer I, Keller H, Leupin O, Kneissel M (2010a) Does osteocytic SOST suppression mediate PTH bone anabolism? Trends Endocrinol. Metab 21, 237-244.
42. Kramer I, Loots GG, Studer A, Keller H, Kneissel M (2010b) Parathyroid hormone (PTH) induced bone gain is blunted in SOST overexpressing and deficient mice. J. Bone Miner. Res. 25, 178-189.
43. Langer M, Prisby R, Peter Z, Boistel R, Lafage-Proust MH, Peyrin F (2009) Quantitative investigation of bone microvascularization from 3D synchrotron micro-computed tomography in a rat model. Conf. Proc. IEEE Eng. Med. Biol. Soc. 1, 1004-1007.
44. Lean JM, Davies JT, Fuller K, Jagger CJ, Kirstein B, Partington GA, Urry ZL, Chambers TJ (2003) A crucial role for thiol antioxidants in estrogen-deficiency bone loss. J. Clin. Invest. 112, 915-923.
45. Lecka-Czernik B, Gubrij I, Moerman EJ, Kajkenova O, Lipschitz DA, Manolagas SC, Jilka RL (1999) Inhibition of Osf2/Cbfa1 expression and terminal osteoblast differentiation by PPARγ2. J. Cell. Biochem. 74, 357-371.
46. Lindsay R, Cosman F, Zhou H, Bostrom MP, Shen VW, Cruz JD, Nieves JW, Dempster DW (2006) A novel tetracycline labeling schedule for longitudinal evaluation of the short-term effects of anabolic therapy with a single iliac crest bone biopsy: early actions of teriparatide. J. Bone Miner. Res. 21, 366-373.
47. Lips P, Courpron P, Meunier PJ (1978) Mean wall thickness of trabecular bone packets in the human iliac crest: changes with age. Calcif. Tissue Res. 26, 13-17.
48. -δδCT method. Methods 25, 402-408.
49. Ma YL, Zeng Q, Donley DW, Ste-Marie LG, Gallagher JC, Dalsky GP, Marcus R, Eriksen EF (2006) Teriparatide increases bone formation in modeling and remodeling osteons and enhances IGF-II immunoreactivity in postmenopausal women with osteoporosis. J. Bone Miner. Res. 21, 855-864.
50. Manolagas SC (2000) Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr. Rev. 21, 115-137.
51. Manolagas SC (2010) From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocr. Rev. 31, 266-300.
52. Manolagas SC, Parfitt AM (2010) What old means to bone. Trends Endocrinol. Metab. 21, 369-374.
53. Marcus R, Wang O, Satterwhite J, Mitlak B (2003) The skeletal response to teriparatide is largely independent of age, initial bone mineral density, and prevalent vertebral fractures in postmenopausal women with osteoporosis. J. Bone Miner. Res. 18, 18-23.
54. Martin-Millan M, Almeida M, Ambrogini E, Han L, Zhao H, Weinstein RS, Jilka RL, O'Brien CA, Manolagas SC (2010) The estrogen receptor-α in osteoclasts mediates the protective effects of estrogens on cancellous but not cortical bone. Mol. Endocrinol. 24, 323-334.
55. O'Brien CA, Plotkin LI, Galli C, Goellner JJ, Gortazar AR, Allen MR, Robling A, Bouxsein M, Schipani E, Turner CH, Jilka RL, Weinstein RS, Manolagas SC, Bellido T (2008) Control of bone mass and remodeling by PTH receptor signaling in osteocytes. PLoS ONE 3, e2942 doi:.
56. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 2, 595-610.
57. Shc. Science 315, 659-663.
58. Potts JT (2005) Parathyroid hormone: past and present. J. Endocrinol. 187, 311-325.
59. Recker RR, Bare SP, Smith SY, Varela A, Miller MA, Morris SA, Fox J (2009) Cancellous and cortical bone architecture and turnover at the iliac crest of postmenopausal osteoporotic women treated with parathyroid hormone 1-84. Bone 44, 113-119.
60. Riggs BL, Parfitt AM (2005) Drugs used to treat osteoporosis: the critical need for a uniform nomenclature based on their action on bone remodeling. J. Bone Miner. Res. 20, 177-184.
61. Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, McDaniel L, Amin S, Rouleau PA, Khosla S (2008) A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J. Bone Miner. Res. 23, 205-214.
62. 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.
63. Saag KG, Zanchetta JR, Devogelaer JP, Adler RA, Eastell R, See K, Krege JH, Krohn K, Warner MR (2009) Effects of teriparatide versus alendronate for treating glucocorticoid-induced osteoporosis: thirty-six-month results of a randomized, double-blind, controlled trial. Arthritis Rheum. 60, 3346-3355.
64. Samadfam R, Xia Q, Goltzman D (2007) Pretreatment with anticatabolic agents blunts but does not eliminate the skeletal anabolic response to parathyroid hormone in oophorectomized mice. Endocrinology 148, 2778-2787.
65. Schneider C, Porter NA, Brash AR (2008) Routes to 4-hydroxynonenal: fundamental issues in the mechanisms of lipid peroxidation. J. Biol. Chem. 283, 15539-15543.
66. Seiler A, Schneider M, Forster H, Roth S, Wirth EK, Culmsee C, Plesnila N, Kremmer E, Radmark O, Wurst W, Bornkamm GW, Schweizer U, Conrad M (2008) Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death. Cell Metab. 8, 237-248.
67. Wan M, Yang C, Li J, Wu X, Yuan H, Ma H, He X, Nie S, Chang C, Cao X (2008) Parathyroid hormone signaling through low-density lipoprotein-related protein 6. Genes Dev. 22, 2968-2979.
68. Weinstein RS, Jilka RL, Almeida M, Roberson PK, Manolagas SC (2010a) Intermittent parathyroid hormone administration counteracts the adverse effects of glucocorticoids on osteoblast and osteocyte viability, bone formation, and strength in mice. Endocrinology 151, 2641-2649.
69. Weinstein RS, Wan C, Liu Q, Wang Y, Almeida M, O'Brien CA, Thostenson J, Roberson PK, Boskey AL, Clemens TL, Manolagas SC (2010b) Endogenous glucocorticoids decrease skeletal angiogenesis, vascularity, hydration, and strength in 21-month-old mice. Aging Cell 9, 147-161.