Trans-10,cis-12 CLA promotes osteoblastogenesis via SMAD mediated mechanism in bone marrow mesenchymal stem cells

Journal of Functional Foods

Volumn 8, Issue 1, 2014, Pages 367-376

  Kim, Jonggun ^a   Park, Yooheon ^a   Park, Yeonhwa ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Adipogenesis; Cis 9,trans 11 CLA; CLA; Osteoblastogenesis; Trans 10,cis 12 CLA

Indexed keywords

EID: 84899922740     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2014.04.006     Document Type: Article

References (74)

1. Akune T., Ohba S., Kamekura S., Yamaguchi M., Chung U.I., Kubota N., Terauchi Y., Harada Y., Azuma Y., Nakamura K., Kadowaki T., Kawaguchi H. PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. The Journal of Clinical Investigation 2004, 113:846-855.
2. Ammann P., Rizzoli R. Bone strength and its determinants. Osteoporosis International: A Journal Established as Result of Cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 2003, 14(Suppl. 3):S13-S18.
3. Arnold S.J., Maretto S., Islam A., Bikoff E.K., Robertson E.J. Dose-dependent Smad1, Smad5 and Smad8 signaling in the early mouse embryo. Developmental Biology 2006, 296:104-118.
4. Banu J., Bhattacharya A., Rahman M., O'Shea M., Fernandes G. Effects of conjugated linoleic acid and exercise on bone mass in young male Balb/C mice. Lipids in Health and Disease [Electronic Resource] 2006, 5:7.
5. Banu J., Bhattacharya A., Rahman M., Fernandes G. Beneficial effects of conjugated linoleic acid and exercise on bone of middle-aged female mice. Journal of Bone and Mineral Metabolism 2008, 26:436-445.
6. Belury M.A., Vanden Heuvel J.P. Advances in conjugated linoleic acid research. Modulation of diabetes by conjugated linoleic acid 1999, Vol. 1:404-411. Chapter 32, AOCS Press, Champaign.
7. Bennett C.N., Longo K.A., Wright W.S., Suva L.J., Lane T.F., Hankenson K.D., MacDougald O.A. Regulation of osteoblastogenesis and bone mass by Wnt10b. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:3324-3329.
8. Bennett C.N., Ouyang H., Ma Y.L., Zeng Q., Gerin I., Sousa K.M., Lane T.F., Krishnan V., Hankenson K.D., MacDougald O.A. Wnt10b increases postnatal bone formation by enhancing osteoblast differentiation. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research 2007, 22:1924-1932.
9. Berge G.M., Ruyter B., Asgard T. Conjugated linoleic acid in diets for juvenile Atlantic salmon (Salmo salar); effects on fish performance, proximate composition, fatty acid and mineral content. Aquaculture (Amsterdam, Netherlands) 2004, 237:365-380.
10. Binato R., Alvarez Martinez C.E., Pizzatti L., Robert B., Abdelhay E. SMAD 8 binding to mice Msx1 basal promoter is required for transcriptional activation. The Biochemical Journal 2006, 393:141-150.
11. Boyle W.J., Simonet W.S., Lacey D.L. Osteoclast differentiation and activation. Nature 2003, 423:337-342.
12. Brown J.M., Boysen M.S., Jensen S.S., Morrison R.F., Storkson J., Lea-Currie R., Pariza M., Mandrup S., McIntosh M.K. Isomer-specific regulation of metabolism and PPARgamma signaling by CLA in human preadipocytes. Journal of Lipid Research 2003, 44:1287-1300.
13. Brownbill R.A., Petrosian M., Ilich J.Z. Association between dietary conjugated linoleic acid and bone mineral density in postmenopausal women. Journal of the American College of Nutrition 2005, 24:177-181.
14. Burr L.L., Taylor C.G., Weiler H.A. Dietary conjugated linoleic acid does not adversely affect bone mass in obese fa/fa or lean Zucker rats. Experimental Biology and Medicine (Maywood, N.J.) 2006, 231:1602-1609.
15. Chin S.F., Storkson J.M., Ha Y.L., Pariza M.W. Dietary sources of conjugated dienoic isomers of linoleic acid. Journal of Food Composition and Analysis 1992, 5:185-197.
16. Dilzer A., Park Y. Implication of conjugated linoleic acid (CLA) in human health. Critical Reviews in Food Science and Nutrition 2012, 52:488-513.
17. Gerstenfeld L.C., Chipman S.D., Glowacki J., Lian J.B. Expression of differentiated function by mineralizing cultures of chicken osteoblasts. Developmental Biology 1987, 122:49-60.
18. Giese K., Pagel J., Grosschedl R. Functional analysis of DNA bending and unwinding by the high mobility group domain of LEF-1. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:12845-12850.
19. Granlund L., Juvet L.K., Pedersen J.I., Nebb H.I. Trans10, cis12-conjugated linoleic acid prevents triacylglycerol accumulation in adipocytes by acting as a PPARgamma modulator. Journal of Lipid Research 2003, 44:1441-1452.
20. Halade G.V., Rahman M.M., Williams P.J., Fernandes G. Combination of conjugated linoleic acid with fish oil prevents age-associated bone marrow adiposity in C57Bl/6J mice. The Journal of Nutritional Biochemistry 2011, 22:459-469.
21. Harada H., Tagashira S., Fujiwara M., Ogawa S., Katsumata T., Yamaguchi A., Komori T., Nakatsuka M. Cbfa1 isoforms exert functional differences in osteoblast differentiation. The Journal of Biological Chemistry 1999, 274:6972-6978.
22. Herbel B.K., McGuire M.K., McGuire M.A., Shultz T.D. Safflower oil consumption does not increase plasma conjugated linoleic acid concentrations in humans. The American Journal of Clinical Nutrition 1998, 67:332-337.
23. Hill C.S. Nucleocytoplasmic shuttling of Smad proteins. Cell Research 2009, 19:36-46.
24. Hillel J.G. An improved automated procedure for the determination of calcium in biological specimens. Analytical Biochemistry 1967, 18:521-531.
25. Iwamoto J., Sato Y., Takeda T., Matsumoto H. Role of sport and exercise in the maintenance of female bone health. Journal of Bone and Mineral Metabolism 2009, 27:530-537.
26. Jewell C., Cusack S., Cashman K.D. The effect of conjugated linoleic acid on transepithelial calcium transport and mediators of paracellular permeability in human intestinal-like Caco-2 cells. Prostaglandins, Leukotrienes, and Essential Fatty Acids 2005, 72:163-171.
27. Katagiri T., Yamaguchi A., Komaki M., Abe E., Takahashi N., Ikeda T., Rosen V., Wozney J.M., Fujisawa-Sehara A., Suda T. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. The Journal of Cell Biology 1994, 127:1755-1766.
28. Kelly O., Cusack S., Jewell C., Cashman K.D. The effect of polyunsaturated fatty acids, including conjugated linoleic acid, on calcium absorption and bone metabolism and composition in young growing rats. The British Journal of Nutrition 2003, 90:743-750.
29. Kim J.H., Kim J., Park Y. trans-10,cis-12 conjugated linoleic acid enhances endurance capacity by increasing fatty acid oxidation and reducing glycogen utilization in mice. Lipids 2012, 47:855-863.
30. Kim J., Park Y., Lee S.H., Park Y. trans-10,cis-12 Conjugated linoleic acid promotes bone formation by inhibiting adipogenesis by peroxisome proliferator activated receptor-gamma-dependent mechanisms and by directly enhancing osteoblastogenesis from bone marrow mesenchymal stem cells. The Journal of Nutritional Biochemistry 2013, 24:672-679.
31. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., Sato M., Okamoto R., Kitamura Y., Yoshiki S., Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89:755-764.
32. Kreider R.B., Ferreira M.P., Greenwood M., Wilson M., Almada A.L. Effects of conjugated linoleic acid supplementation during resistance training on body composition, bone density, strength, and selected hematological markers. Journal of Strength and Conditioning Research 2002, 16:325-334.
33. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336.
34. Lee K.S., Kim H.J., Li Q.L., Chi X.Z., Ueta C., Komori T., Wozney J.M., Kim E.G., Choi J.Y., Ryoo H.M., Bae S.C. Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Molecular and Cellular Biology 2000, 20:8783-8792.
35. Li B. Bone morphogenetic protein-Smad pathway as drug targets for osteoporosis and cancer therapy. Endocrine, Metabolic & Immune Disorders Drug Targets 2008, 8:208-219.
36. Mackie E.J. Osteoblasts: Novel roles in orchestration of skeletal architecture. The International Journal of Biochemistry & Cell Biology 2003, 35:1301-1305.
37. Martin T.J., Ng K.W. Mechanisms by which cells of the osteoblast lineage control osteoclast formation and activity. Journal of Cellular Biochemistry 1994, 56:357-366.
38. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes & Development 2005, 19:2783-2810.
39. Mbalaviele G., Sheikh S., Stains J.P., Salazar V.S., Cheng S.L., Chen D., Civitelli R. Beta-catenin and BMP-2 synergize to promote osteoblast differentiation and new bone formation. Journal of Cellular Biochemistry 2005, 94:403-418.
40. Mele M.C., Cannelli G., Carta G., Cordeddu L., Melis M.P., Murru E., Stanton C., Banni S. Metabolism of c9,t11-conjugated linoleic acid (CLA) in humans. Prostaglandins, Leukotrienes, and Essential Fatty Acids 2013, 89:115-119.
41. Mizutani A., Sugiyama I., Kuno E., Matsunaga S., Tsukagoshi N. Expression of matrix metalloproteinases during ascorbate-induced differentiation of osteoblastic MC3T3-E1 cells. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research 2001, 16:2043-2049.
42. National Osteoporosis Foundation Bone Health Basics: Get the Facts accessed May 2013. http://www.nof.org/learn.
43. Nelson-Dooley C., Della-Fera M.A., Hamrick M., Baile C.A. Novel treatments for obesity and osteoporosis: Targeting apoptotic pathways in adipocytes. Current Medicinal Chemistry 2005, 12:2215-2225.
44. Owen T.A., Aronow M., Shalhoub V., Barone L.M., Wilming L., Tassinari M.S., Kennedy M.B., Pockwinse S., Lian J.B., Stein G.S. Progressive development of the rat osteoblast phenotype in vitro: Reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. Journal of Cellular Physiology 1990, 143:420-430.
45. Pan L.C., Price P.A. The propeptide of rat bone gamma-carboxyglutamic acid protein shares homology with other vitamin K-dependent protein precursors. Proceedings of the National Academy of Sciences of the United States of America 1985, 82:6109-6113.
46. Pandur P., Maurus D., Kuhl M. Increasingly complex: New players enter the Wnt signaling network. Bioessays: News and Reviews in Molecular, Cellular and Developmental Biology 2002, 24:881-884.
47. Park Y., Albright K.J., Liu W., Storkson J.M., Cook M.E., Pariza M.W. Effect of conjugated linoleic acid on body composition in mice. Lipids 1997, 32:853-858.
48. Park Y., McGuire M.K., Behr R., McGuire M.A., Evans M.A., Shultz T.D. High-fat dairy product consumption increases delta 9c,11t-18:2 (rumenic acid) and total lipid concentrations of human milk. Lipids 1999, 34:543-549.
49. Park Y., Storkson J.M., Albright K.J., Liu W., Pariza M.W. Evidence that the trans-10,cis-12 isomer of conjugated linoleic acid induces body composition changes in mice. Lipids 1999, 34:235-241.
50. Park Y., Storkson J.M., Ntambi J.M., Cook M.E., Sih C.J., Pariza M.W. Inhibition of hepatic stearoyl-CoA desaturase activity by trans-10, cis-12 conjugated linoleic acid and its derivatives. Biochimica et Biophysica Acta 2000, 1486:285-292.
51. Park Y., Pariza M.W. Mechanisms of body fat modulation by conjugated linoleic acid (CLA). Food Research International 2007, 40:311-323.
52. Park Y., Pariza M.W., Park Y. Co-supplementation of dietary calcium and conjugated linoleic acid (CLA) improves bone mass in mice. Journal of Food Science 2008, 73:C556-C560.
53. Park Y., Park Y. Conjugated nonadecadienoic acid is more potent than conjugated linoleic acid on body fat reduction. The Journal of Nutritional Biochemistry 2010, 21:764-773.
54. Park Y., Terk M., Park Y. Interaction between dietary conjugated linoleic acid and calcium supplementation affecting bone and fat mass. Journal of Bone and Mineral Metabolism 2011, 29:268-278.
55. Park Y., Park Y. Conjugated fatty acids increase energy expenditure in part by increasing voluntary movement in mice. Food Chemistry 2012, 133:400-409.
56. Pigozzi F., Rizzo M., Giombini A., Parisi A., Fagnani F., Borrione P. Bone mineral density and sport: Effect of physical activity. The Journal of Sports Medicine and Physical Fitness 2009, 49:177-183.
57. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., Moorman M.A., Simonetti D.W., Craig S., Marshak D.R. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
58. Platt I.D., El-Sohemy A. Regulation of osteoblast and adipocyte differentiation from human mesenchymal stem cells by conjugated linoleic acid. The Journal of Nutritional Biochemistry 2009, 20:956-964.
59. Rahman M.M., Bhattacharya A., Banu J., Fernandes G. Conjugated linoleic acid protects against age-associated bone loss in C57BL/6 female mice. The Journal of Nutritional Biochemistry 2007, 18:467-474.
60. Rahman M.M., Bhattacharya A., Fernandes G. Conjugated linoleic acid inhibits osteoclast differentiation of RAW264.7 cells by modulating RANKL signaling. Journal of Lipid Research 2006, 47:1739-1748.
61. Rahman M.M., Halade G.V., Williams P.J., Fernandes G. t10c12-CLA maintains higher bone mineral density during aging by modulating osteoclastogenesis and bone marrow adiposity. Journal of Cellular Physiology 2011, 226:2406-2414.
62. Rawadi G. Wnt signaling and potential applications in bone diseases. Current Drug Targets 2008, 9:581-590.
63. Ritzenthaler K., McGuire M., Falen R., Shultz T., McGuire M. Estimation of conjugated linoleic acid (CLA) intake. Faseb Journal 1998, 12:A527.
64. Roche H.M., Terres A.M., Black I.B., Gibney M.J., Kelleher D. Fatty acids and epithelial permeability: Effect of conjugated linoleic acid in Caco-2 cells. Gut 2001, 48:797-802.
65. Roy B.D., Bourgeois J., Rodriguez C., Payne E., Young K., Shaughnessy S.G., Tarnopolosky M.A. Conjugated linoleic acid prevents growth attenuation induced by corticosteroid administration and increases bone mineral content in young rats. Applied Physiology, Nutrition, and Metabolism = Physiologie Appliquee, Nutrition Et Metabolisme 2008, 33:1096-1104.
66. Seeman E. Reduced bone formation and increased bone resorption: Rational targets for the treatment of osteoporosis. Osteoporosis International: A Journal Established as Result of Cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 2003, 14(Suppl. 3):S2-S8.
67. Suda T., Takahashi N., Udagawa N., Jimi E., Gillespie M.T., Martin T.J. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocrine Reviews 1999, 20:345-357.
68. Takada I., Suzawa M., Matsumoto K., Kato S. Suppression of PPAR transactivation switches cell fate of bone marrow stem cells from adipocytes into osteoblasts. Annals of the New York Academy of Sciences 2007, 1116:182-195.
69. Terpstra A.H. Differences between humans and mice in efficacy of the body fat lowering effect of conjugated linoleic acid: Role of metabolic rate. The Journal of Nutrition 2001, 131:2067-2068.
70. Watkins B.A., Shen C.L., McMurtry J.P., Xu H., Bain S.D., Allen K.G., Seifert M.F. Dietary lipids modulate bone prostaglandin E2 production, insulin-like growth factor-I concentration and formation rate in chicks. The Journal of Nutrition 1997, 127:1084-1091.
71. Weiler H.A., Fitzpatrick S., Fitzpatrick-Wong S.C. Dietary conjugated linoleic acid in the cis-9, trans-11 isoform reduces parathyroid hormone in male, but not female, rats. The Journal of Nutritional Biochemistry 2008, 19:762-769.
72. Whyte M.P. Physiological role of alkaline phosphatase explored in hypophosphatasia. Annals of the New York Academy of Sciences 2010, 1192:190-200.
73. Wolff I., van Croonenborg J.J., Kemper H.C., Kostense P.J., Twisk J.W. The effect of exercise training programs on bone mass: A meta-analysis of published controlled trials in pre- and postmenopausal women. Osteoporosis International: A Journal Established as Result of Cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 1999, 9:1-12.
74. Wozney J.M., Rosen V. Bone morphogenetic protein and bone morphogenetic protein gene family in bone formation and repair. Clinical Orthopaedics and Related Research 1998, 346:26-37.