Hedgehog signaling and osteogenic differentiation in multipotent bone marrow stromal cells are inhibited by oxidative stress

Journal of Cellular Biochemistry

Volumn 111, Issue 5, 2010, Pages 1199-1209

  Kim, Woo Kyun ^a   Meliton, Vicente ^a   Bourquard, Noam ^a   Hahn, Theodore J ^b   Parhami, Farhad ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

Author keywords

Hedgehog; mesenchymal stem cells; osteogenesis; oxidative stress

Indexed keywords

ALKALINE PHOSPHATASE; BONE SIALOPROTEIN; HYDROGEN PEROXIDE; OXIDIZED LOW DENSITY LIPOPROTEIN; PROTEIN PATCHED 1; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; TRANSCRIPTION FACTOR OSTERIX; XANTHINE OXIDASE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BONE AGE; BONE DEVELOPMENT; BONE MARROW CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; FIBROBLAST; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; MOUSE; MULTIPOTENT BONE MARROW STROMAL CELL; NONHUMAN; OSTEOBLAST; OSTEOPOROSIS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STROMA CELL;

ANIMALS; BIOLOGICAL MARKERS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; HEDGEHOG PROTEINS; MICE; OSTEOBLASTS; OSTEOGENESIS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; STROMAL CELLS;

ERINACEIDAE;

EID: 78649875480     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22846     Document Type: Article

References (51)

1. Alaiwi WAA, Lo ST, Mauli SM,. 2009. Primary cilia: Highly sophisticated biological sensors. Sensors 9: 7003-7020.
2. 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,. 2007. Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 282: 27285-27297.
3. Almeida M, Ambrogini E, Han L, Manolagas SC, Jilka RL,. 2009. Increased lipid oxidation causes oxidative stress, increased peroxisome proliferator-activated receptor-γ expression, and diminished pro-osteogenic Wnt signaling in the skeleton. J Biol Chem 284: 27438-27448.
4. Aoto K, Shikata Y, Higashiyama D, Shiota K, Motoyama J,. 2008. Fetal ethanol exposure activates protein kinase A and impairs Shh expression in prechordal mesendoderm cells in the pathogenesis of holoprosencephaly. Birth Defects Res A Clin Mol Teratol 82: 224-231.
5. Basu S, Michaelsson K, Olofsson H, Johansson S, Melhus H,. 2001. Association between oxidative stress and bone mineral density. Biochem Biophy Res Comm 288: 275-279.
6. Beachy PA, Karhadkar SS, Berman DM,. 2004. Tissue repair and stem cell renewal in carcinogenesis. Nature 432: 324-331.
7. Beckers L, Heeneman S, Wang L, Burkly LC, Rousch MMJ, Davidson NO, Gijbels MJJ, de Winther MPJ, Daemen MJAP, Lutgens E,. 2007. Disruption of Hedgehog signaling in ApoE-/- mice reduces plasma lipid levels, but increases atherosclerosis due to enhanced lipid uptake by macrophages. J Pathol 212: 420-428.
8. Beresford JN, Bennett JH, Devin C, Leboy PS, Owen ME,. 1992. Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci 102: 341-351.
9. Chan GK, Duque G,. 2002. Age-related bone loss: Old bone, new facts. Gerontology 48: 62-71.
10. Chen XD, Shi S, Xu T, Robey PG, Young MF,. 2002. Age-related osteoporosis in biglycan-deficient mice is related to defects in bone marrow stromal cells. J Bone Miner Res 17: 331-340.
11. Cummings SR, Melton LJ III., 2002. Epidemiology and outcomes of osteoporotic fractures. Lancet 359: 1761-1767.
12. Cuschieri J, Maier RV,. 2007. Oxidative stress, lipid rafts, and macrophage reprogramming. Antioxid Redox Signal 9: 1485-1497.
13. D'ippolito G, Schiller PC, Ricordi C, Roos BA, Howard G,. 1999. Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow. J Bone Miner Res 14: 1115-1122.
14. Dennery PA,. 2007. Effects of oxidative stress on embryonic development. Birth Defects Res 81: 155-162.
15. Dwyer JR, Sever N, Carlson M, Nelson SF, Beachy PA, Pahami F,. 2007. Oxysterols are novel activators of the hedgehog signaling pathway in pluripotent mesenchymal cells. J Biol Chem 282: 8959-8968.
16. Ehlen HWA, Buelens LA, Vortkamp A,. 2006. Hedgehog signaling in skeletal development. Birth Defects Res 78: 267-279.
17. Garrett IR, Boyce BF, Oreffo ROC, Bonewald L, Poser J, Mundy GR,. 1990. Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 85: 632-639.
18. Girotti AW,. 2001. Phoosensitized oxidation of membrane lipids: Reaction pathways, cytotoxic effects, and cytoprotective mechanisms. J Photochem Photobiol B 63: 103-113.
19. Haycraft CJ, Zhang Q, Song B, Jackson WS, Detloff PJ, Serra R, Yoder BK,. 2007. Intraflagellar transport is essential for endochondral bone formation. Development 134: 307-316.
20. Huangfu D, Anderson KV,. 2005. Cilia and Hedgehog responsiveness in the mouse. Proc Nat Acad Sci 102: 11325-11330.
21. Ito H, Akiyama H, Shigeno C, Iyama K, Matsuoka H, Nakamura T,. 1999. Hedgehog signaling molecules in bone marrow cells at the initial stage of fracture repair. Biochem Biophys Res Comm 262: 443-451.
22. Joseph JA, Denisova N, Fisher D, Shukitt-Hale B, Bickford P, Prior R, Cao G,. 1998. Membrane and receptor modifications of oxidative stress vulnerability in aging. Nutritional considerations. Ann NY Acad Sci 854: 268-276.
23. Kha HT, Basseri B, Shouhed D, Richardson J, Tetradis S, Hahn TJ, Parhami F,. 2004. Oxysterols regulate differentiation of mesenchymal stem cells: Pro-bone and anti-fat. J Bone Miner Res 19: 830-840.
24. Kim WK, Meliton V, Park KW, Hong C, Tontonoz P, Niewiadomski P, Waschek JA, Tetradis S, Parhami F,. 2009. Negative regulation of Hedgehog signaling by liver X receptors. Mol Endocrinol 23: 1532-1543.
25. Kimura H, Ng JMY, Curran T,. 2008. Transient inhibition of the hedgehog pathway in young mice cause permanent defects in bone structure. Cancer Cell 13: 249-260.
26. Maggio D, Barabani M, Pierandrei M, Polidori MC, Catani M, Mecocci P, Senin U, Pacifici R, Cherubini A,. 2003. Marked decrease in plasma antioxidants in aged osteoporotic women: Results of a cross-sectional study. Clin Endocrinol Metab 88: 1523-1527.
27. May SR, Ashique AM, Karlen M, Wang B, Shen Y, Zarbalis K, Reiter J, Ericson J, Peterson AS,. 2005. Loss of the retrograde motor for IFT disrupts localization of Smo to cilia and prevents the expression of both activator and repressor functions of Gli. Dev Bio 287: 378-389.
28. McMahon AP, Ingham PW, Tabin CJ,. 2003. Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 53: 1-114.
29. Meunier P, Aaron J, Edouard C, Vignon G,. 1971. Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop 80: 147-154.
30. Michaud EJ, Yoder BK,. 2006. The primary cilium in cell signaling and cancer. Cancer Res 66: 6463-6467.
31. Milenkovic L, Scott MP, Rohatgi R,. 2009. Lateral transport of Smoothened from the plasma membrane to the membrane of the cilum. J Cell Biol 187: 365-374.
32. Mody N, Parhami F, Sarafian TA, Demer LL,. 2001. Differential effects of oxidative stress on osteoblastic differentiation of vascular and bone cells. Free Radic Res Med 31: 509-519.
33. Nuttall ME, Patton AJ, Olivera DL, Nadeau DP, Gowen M,. 1998. Human trabecular bone cells are able to express both osteoblastic and adipocytic phenotype: Implications for osteopenic disorders. J Bone Miner Res 13: 371-382.
34. Orozco LD, Kapturczak MH, Barajas B, Wang X, Weinstein MM, Wong J, Deshane J, Biolisetty S, Shaposhnik Z, Shih DM, Agarwal A, Lusis AJ, Araujo JA,. 2007. Heme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis. Circ Res 100: 1703-1711.
35. Parhami F,. 2003. Possible role of oxidized lipids in osteoporosis: Could hyperlipidemia be a rish factor? Prostaglandins Leukot Essent Fatty Acids 68: 373-378.
36. Parhami F, Morrow AD, Balucan J, Leitinger N, Watson AD, Tintut Y, Berliner JA, Demer LL,. 1997. Lipid oxidation products have opposite effects on calcifying vascular cell and bone cell differentiation: A possible explanation for the paradox of arterial calcification in osteoporotic patients. Arterioscler Thromb Vasc Biol 17: 680-687.
37. Parhami F, Jackson SM, Tintut Y, Le V, Balucan JP, Territo M, Demer LL,. 1999. Atherogenic diet and minimally oxidized low density lipoprotein inhibit osteogenic and promote adipogenic differentiation of marrow stromal cells. J Bone Miner Res 14: 2067-2078.
38. Parhami F, Tintut Y, Beamer WG, Gharavi N, Goodman W, Demer LL,. 2001. Atherogenic high-fat diet reduces bone mineralization in mice. J Bone Min Res 16: 182-188.
39. Richardson JA, Amantea CM, Kianmahd B, Tetradis S, Lieberman JR, Hahn TJ, Parhami F,. 2007. Oxysterol-induced osteoblastic differentiation of pluripotent mesenchymal cells is mediated through a PKC- and PKA-dependent pathway. J Cell Biochem 100: 1131-1145.
40. Rohatgi R, Scott MP,. 2007. Patching the gaps in Hedgehog signaling. Nature Cell Bio 9: 1005-1009.
41. Rohatgi R, Milenkovic L, Scott MP,. 2007. Patched1 regulates Hedgehog signaling at the primary cilium. Science 317: 372-376.
42. Rosenfeld ME,. 1991. Oxidized LDL affects multiple atherogenic cellular responses. Circulation 83: 2137-2140.
43. Shouhed D, Kha HT, Richardson JA, Amantea CM, Hahn TJ, Parhami F,. 2005. Osteogenic oxysterols inhibit the adverse effects of oxidative stress on osteogenic differentiation of marrow stromal cells. J Cell Biochem 95: 1276-1283.
44. Simons M, Gloy J, Ganner A, Bullerkotte A, Bashkurov M, Kronig C, Schermer B, Benzing T, Cabello OA, Jenny A, Mlodzik M, Polok B, Briever W, Obara T, Walz G,. 2005. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 37: 537-543.
45. Sinha S, Chen JK,. 2006. Purmorphamine activates the Hedgehog pathway by targeting Smoothened. Nature Chem Biol 2: 29-30.
46. Spinella-Jaegle S, Rawad G, Kawai S, Gallea S, Faucheu C, Mollat P, Courtois B, Bergaud B, Ramez V, Blanche AM, Adelmant G, Baron R, Roman-Roman S,. 2001. Sonic hedgehog increases the commitment of pluripotent mesenchymal cells into the osteoblastic lineage and abolishes adipocytic differentiation. J Cell Sci 114: 2085-2094.
47. Stark G,. 2005. Functional consequences of oxidative membrane damage. J Membr Biol 205: 1-16.
48. Suh JM, Gao X, McKay J, McKay R, Salo Z, Graff JM,. 2006. Hedgehog signaling plays a conserved role in inhibiting fat formation. Cell Metab 3: 25-34.
49. Taipale J, Chen JK, Cooper MK, Wang B, Mann RK, Milenkovic L, Scott MP, Beachy PA,. 2000. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406: 1005-1009.
50. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J,. 2007. Free radicals and antioxidants in normal physiological functions and human disease. Int J Bio Cell Biol 39: 44-84.
51. Wong SY, Seol AD, So PL, Ermilov AN, Bichakjian CK, Epstein EH, Dlugosz AA, Reiter JF,. 2009. Primary cilia can both mediate and suppress Hedgehog pathway-dependent tumorogenesis. Nature Med 15: 1055-1061.