Depot-specific and hypercaloric diet-induced effects on the osteoblast and adipocyte differentiation potential of adipose-derived stromal cells

Molecular and Cellular Endocrinology

Volumn 348, Issue 1, 2012, Pages 55-66

  Sadie Van Gijsen, Hanel ^a   Smith, Wayne ^a   du Toit, Eugene Francois ^a   Michie, John ^a   Hough, F S ^a   Ferris, William Frank ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Adipocyte differentiation; Adipose depots; Adipose derived stromal cells; Diet induced obesity; Msx2; Osteoblast differentiation

Indexed keywords

TRANSCRIPTION FACTOR MSX2;

ADIPOCYTE; ADIPOSE DERIVED STROMAL CELL; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; IN VIVO STUDY; INTRAABDOMINAL FAT; METABOLIC DISORDER; NONHUMAN; OBESITY; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STROMA CELL; SUBCUTANEOUS FAT;

ADIPOCYTES; ADIPOSE TISSUE; ALKALINE PHOSPHATASE; ANIMALS; ANTIGENS, DIFFERENTIATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SHAPE; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 1 SUBUNIT; ENERGY INTAKE; GENE EXPRESSION; HOMEODOMAIN PROTEINS; INTEGRIN-BINDING SIALOPROTEIN; MALE; OBESITY; OSTEOBLASTS; RATS; RATS, WISTAR; STROMAL CELLS;

EID: 84860391255     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.07.030     Document Type: Article

References (76)

1. Afghani A., Goran M.I. The interrelationships between abdominal adiposity, leptin and bone mineral content in overweight Latino children. Horm. Res. 2009, 72:82-87.
2. Allan E.H., Ho P.W., Umezawa A., Hata J., Makishima F., Gillespie M.T., Martin T.J. Differentiation potential of a mouse bone marrow stromal cell line. J. Cell. Biochem. 2003, 90(1):158-169.
3. Bielohuby M., Matsuura M., Herbach N., Kienzle E., Slawik M., Hoeflich A., Bidlingmaier M. Short term exposure to low-carbohydrate/high-fat diets induces low bone mineral density and reduces bone formation in rats. J. Bone Miner. Res. 2009, 25:275-284.
4. Blaauw R., Albertse E.C., Hough S. Body fat distribution as a risk factor for osteoporosis. S. Afr. Med. J. 1996, 86:1081-1084.
5. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
6. Cave M. Incorporation of tritium-labelled thymidine and lysine into chromosomes of cultured human leukocytes. J. Cell Biol. 1966, 29:209-222.
7. Centers for Disease Control, Prevention, Prevalence of overweight and obesity among adults with diagnosed diabetes - United States, 1988-2004 and 1999-2002. Morb. Mortal. Wkly Rep. 2004, 53:1066-1068.
8. Cheng S.L., Shao J.S., Charlton-Kachigian N., Loewy A.P., Towler D.A. MSX2 promotes osteogenesis and suppresses adipogenic differentiation of multipotent mesenchymal progenitors. J. Biol. Chem. 2003, 278:45969-45977.
9. Deen D. Metabolic syndrome: time for action. Am. Fam. Physician 2004, 69:2875-2882.
10. De Liefde I.I., Van der Klift M., De Laet C.E., Van Daele P.L., Hofman A., Pols H.A. Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos. Int. 2005, 16:1713-1720.
11. Dennison E.M., Syddall H.E., Aihie Sayer A., Craighead S., Phillips D.I., Cooper C. Type 2 diabetes mellitus is associated with increased axial bone density in men and women from the Hertfordshire Cohort Study: evidence for an indirect effect of insulin resistance?. Diabetologia 2004, 47:1963-1968.
12. De Paula F.J.A., Horowitz M.C., Rosen C.J. Novel insights into the relationship between diabetes and osteoporosis. Diabetes Metab. Res. Rev. 2010, 26:622-630.
13. Ducy P. Cbfa1: a molecular switch in osteoblast biology. Dev. Dyn. 2000, 219:461-471.
14. Du Toit E.F., Smith W., Muller C., Strijdom H., Stouthammer B., Woodiwiss A.J., Norton G.R., Lochner A. Myocardial susceptibility to ischemic-reperfusion injury in a prediabetic model of dietary-induced obesity. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H2336-H2343.
15. Fedarko N.S., D'Avis P., Frazier C.R., Burrill M.J., Fergusson V., Tayback M., Sponseller P.D., Shapiro J.R. Cell proliferation of human fibroblasts and osteogenesis in osteogenesis imperfecta: Influence of age. J. Bone Miner. Res. 1995, 10:1705-1712.
16. Fickert S., Fiedler J., Brenner R.E. Identification of subpopulations with characteristics of mesenchymal progenitor cells from human osteoarthritic cartilage using triple staining for cell surface markers. Arthritis Res. Ther. 2004, 6:R422-R432.
17. Fraser J.K., Wulur I., Alfonso Z., Hedrick M.H. Fat tissue: an underappreciated source of stem cells for biotechnology. Trends Biotechnol. 2006, 24:150-154.
18. Guo R., Yamashita M., Zhang Q., Zhou Q., Chen D., Reynolds D.G., Awad H.A., Yanoso L., Zhao L., Schwarz E.M., Zhang Y.E., Boyce B.F., Xing L. Ubiquitin ligase Smurf1 mediates tumor necrosis factor-induced systemic bone loss by promoting proteasomal degradation of bone morphogenetic signaling proteins. J. Biol. Chem. 2008, 283:23084-23092.
19. Hjelmeland A.B., Schilling S.H., Guo X., Quarles D., Wang X.-F. Loss of Smad3-mediated negative regulation of Runx2 activity leads to an alteration in cell fate determination. Mol. Cell. Biol. 2005, 25:9460-9468.
20. Hodgkinson T., Yuan X.F., Bayat A. Adult stem cells in tissue engineering. Expert Rev. Med. Devices 2009, 6:621-640.
21. Hough F.S. Re: diabetic osteopenia. Diabetes Res. Clin. Pract. 1989, 7:161-162.
22. Huang J.I., Beanes S.R., Zhu M., Lorenz H.P., Hedrick M.H., Benhaim P. Rat extramedullary adipose tissue as a source of osteochondrogenic progenitor cells. Plast. Reconstr. Surg. 2002, 109:1033-1041.
23. Huang M.S., Lu J., Ivanov Y., Sage A.P., Tseng W., Demer L.L., Tintut Y. Hyperlipidaemia impairs osteoanabolic effects of PTH. J. Bone Miner. Res. 2008, 23:1672-1679.
24. Ichida F., Nishimura R., Hata K., Matsubara T., Ikeda F., Hisada K., Yatani H., Cao X., Komori T., Yamaguchi A., Yoneda T. Reciprocal roles of MSX2 in regulation of osteoblast and adipocyte differentiation. J. Biol. Chem. 2004, 279:34015-34022.
25. Jaiswal N., Haynesworth S.E., Caplan A.I., Bruder S.P. Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. J. Cell. Biochem. 1997, 64:295-312.
26. Jankowska E.A., Rogucka E., MedraŚ M. Are general obesity and visceral obesity in men linked to reduced bone mineral content resulting from normal ageing? A population-based study. Andrologia 2001, 33:384-389.
27. Jensen M.D. Role of body fat distribution and the metabolic complications of obesity. J. Clin. Endocrinol. Metab. 2008, 93:S57-S63.
28. Jeon O., Rhie J.W., Kwon I.K., Kim J.H., Kim B.S., Lee S.H. In vivo bone formation following transplantation of human adipose-derived stromal cells that are not differentiated osteogenically. Tissue Eng. Part A 2008, 14:1285-1294.
29. Kato S., Kawabata N., Suzuki N., Ohmura M., Takagi M. Bone morphogenetic protein-2 induces the differentiation of a mesenchymal progenitor cell line, ROB-C26, into mature osteoblasts and adipocytes. Life Sci. 2009, 84:302-310.
30. Kinjo M., Setoguchi S., Solomon D.H. Bone mineral density in adults with the metabolic syndrome: analysis in a population-based US sample. J. Clin. Endocrinol. Metab. 2007, 92:4161-4164.
31. Kishimoto T., Kikutani H., Borne A., Goyert S.M., Mason D., Miyasaki M., Moretta L., Okumura K., Shaw S., Springer T., Sugamura K., Zola H. Leucocyte typing VI, white cell differentiation antigens 1997, Garland Publishing, Hamden, Connecticut.
32. Kotobuki N., Matsushima A., Kato Y., Kubo Y., Hirose M., Ohgushi H. Small interfering RNA of alkaline phosphatase inhibits matrix mineralization. Cell Tissue Res. 2008, 332:279-288.
33. Kuroda S., Virdi A.S., Dai Y., Shott S., Sumner D.R. Patterns and localization of gene expression during intramembranous bone regeneration in the rat femoral marrow ablation model. Calcif. Tissue Int. 2005, 77:212-225.
34. Laughton C. Measurement of the specific lipid content of attached cells in microtitre cultures. Anal. Biochem. 1986, 156:307-314.
35. Lee J.A., Parrett B.M., Conejero J.A., Laser J., Chen J., Kogon A.J., Nanda D., Grant R.T., Breitbart A.S. Biological alchemy: engineering bone and fat from fat-derived stem cells. Ann. Plast. Surg. 2003, 50:610-617.
36. Li W., Yu B., Li M., Sun D., Hu Y., Zhao M., Cui C.B., Hou S. NEMO-binding domain peptide promotes osteoblast differentiation impaired by tumor necrosis factor alpha. Biochem. Biophys. Res. Commun. 2010, 391:1229-1233.
37. Liu Z., Shi W., Ji X., Sun C., Jee W.S., Wu Y., Mao Z., Nagy T.R., Li Q., Cao X. Molecules mimicking Smad1 interacting with Hox stimulate bone formation. J. Biol. Chem. 2004, 279:11313-11319.
38. Matsubara T., Kida K., Yamaguchi A., Hata K., Ichida F., Meguro H., Aburatani H., Nishimura R., Yoneda T. BMP2 regulates Osterix through Msx2 and Runx2 during osteoblast differentiation. J Biol Chem. 2008, 283(43):29119-29125.
39. Merchant-Larios H., Mendlovic F., Alvarez-Buylla A. Characterization of alkaline phosphatase from primordial germ cells and ontogenesis of this enzyme in the mouse. Differentiation 1985, 29:145-151.
40. Nakashima K., Zhou X., Kunkel G., Zhang Z., Deng J.M., Behringer R.R., de Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 2002, 108:17-29.
41. Narisawa S., Wennberg C., Millan J.L. Abnormal vitamin B6 metabolism in alkaline phosphatase knock-out mice causes multiple abnormalities, but not the impaired bone mineralization. J. Pathol. 2001, 193:125-133.
42. Noël D., Caton D., Roche S., Bony C., Lehmann S., Casteilla L., Jorgensen C., Cousin B. Cell specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Exp. Cell Res. 2008, 314:1575-1584.
43. Ogawa R., Mizuno H., Watanabe A., Migita M., Hyakusoku H., Shimada T. Adipogenic differentiation by adipose-derived stem cells harvested from GFP transgenic mice - Including relationship of sex differences. Biochem. Biophys. Res. Commun. 2004, 319:511-517.
44. Ohnishi S., Okabe K., Obata H., Otani K., Ishikane S., Ogino H., Kitamura S., Nagaya N. Involvement of tazarotene-induced gene 1 in proliferation and differentiation of human adipose tissue-derived mesenchymal stem cells. Cell Prolif. 2009, 42:309-316.
45. Orozco P. Atherogenic lipid profile and elevated lipoprotein (a) are associated with lower bone mineral density in early postmenopausal overweight women. Eur. J. Epidemiol. 2004, 19:1105-1112.
46. Parhami F., Jackson S.M., Tintut Y., Le V., Balucan J.P., Territo M., Demer L.L. Atherogenic diet and minimally oxidized low density lipoprotein inhibit osteogenic and promote adipogenic differentiation of marrow stromal cells. J. Bone Miner. Res. 1999, 14:2067-2078.
47. Peptan I.A., Hong L., Mao J.J. Comparison of osteogenic potentials of visceral and subcutaneous adipose-derived cells of rabbits. Plast. Reconstr. Surg. 2006, 117:1462-1470.
48. Pfaffl M. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
49. Phillips J.E., Gersbach C.A., Wojtowicz A.M., Garcia A.J. Glucocorticoid-induced osteogenesis is negatively regulated by Runx2/Cbfa1 serine phosphorylation. J. Cell Sci. 2006, 119:581-591.
50. Pollock N.K., Bernard P.J., Wenger K., Misra S., Gower B.A., Allison J.D., Zhu H., Davis C.L. Lower bone mass in prepubertal overweight children with prediabetes. J Bone Miner Res. 2010, 25(12):2760-2769.
51. Pickavance L.C., Tadayyon M., Widdowson P.S., Buckingham R.E., Wilding J.P.H. Therapeutic index for rosiglitazone in dietary obese rats: separation of efficacy and haemodilution. Br. J. Pharmacol. 1999, 128:1570-1576.
52. Prisby R.D., Swift J.M., Bloomfield S.A., Hogan H.A., Delp M.D. Altered bone mass, geometry and mechanical properties during the development and progression of type 2 diabetes in the Zucker diabetic fatty rat. J Endocrinol. 2008, 199(3):379-388.
53. Reid I.R., Civitelli R., Avioli L.V., Hruska K.A. Parathyroid hormone depresses cytosolic pH and DNA synthesis in osteoblast-like cells. Am. J. Physiol. 1988, 255:E9-E15.
54. Reinholz G.G., Getz B., Pederson L., Sanders E.S., Subramaniam M., Ingle J.N., Spelsberg T.C. Bisphosphonates directly regulate cell proliferation, differentiation, and gene expression in human osteoblasts. Cancer Res. 2000, 60:6001-6007.
55. Rubin C.S., Hirsch A., Fung C., Rosen O.M. Development of hormone receptors and hormone responsiveness in vitro. J. Biol. Chem. 1978, 253:7570-7578.
56. Russell M., Mendes N., Miller K.K., Rosen C.J., Lee H., Kilbanski A., Misra M. Visceral fat is a negative predictor of bone density measures in obese adolescent girls. J. Clin. Endocrinol. Metab. 2010, 95:1247-1255.
57. Sadie-Van Gijsen H., Crowther N., Hough F.S., Ferris W.F. Depot-related differences in the insulin response of adipose-derived stromal cells. Mol. Cell. Endocrinol. 2010, 328:22-27.
58. Satokata I., Ma L., Ohshima H., Bei M., Woo I., Mishizawa K., Maeda T., Takano Y., Uchiyama M., Heaney S., Peters H., Tang Z., Maxson R., Maas R. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat. Genet. 2000, 24:391-395.
59. Shirakabe K., Terasawa K., Miyama K., Shibuya H., Nishida E. Regulation of the activity of the transcription factor Runx2 by two homeobox proteins, Msx2 and Dlx5. Genes Cells 2001, 6:851-856.
60. Smith P.J., Wise L.S., Berkowitz R., Wan C., Rubin C.S. Insulin-like growth factor-1 is an essential regulator of the differentiation of 3T3-L1 adipocytes. J. Biol. Chem. 1988, 263:9402-9408.
61. Song L., Tuan R.S. Transdifferentiation potential of human mesenchymal stem cells derived from bone marrow. FASEB J. 2004, 18:980-982.
62. Stein G.S., Lian J.B. Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype. Endocr. Rev. 1993, 14:424-442.
63. Tanabe N., Ito-Kato E., Suzuki N., Nakayama A., Ogiso B., Maeno M., Ito K. IL-1α affects mineralized nodule formation by rat osteoblasts. Life Sci. 2004, 75:2317-2327.
64. Tanabe Y., Koga M., Saito M., Matsunaga Y., Nakayama K. Inhibition of adipocyte differentiation by mechanical stretching through ERK-mediated downregulation of PPARγ2. J. Cell Sci. 2004, 117:3605-3614.
65. Tholpady S.S., Katz A.J., Ogle R.C. Mesenchymal stem cells from rat visceral fat exhibit multipotential differentiation in vitro. Anat. Rec. A 2003, 272A:398-402.
66. Thrailkill K.M., Lumpkin C.K., Bunn R.C., Kemp S.F., Fowlkes J.L. Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am. J. Physiol. Endocrinol. Metab. 2005, 289:E735-E745.
67. Tomomatsu N., Aoki K., Alles N., Soysa N.S., Hussain A., Nakachi H., Kita S., Shimokawa H., Ohya K., Amagasa T. LPS-induced inhibition of osteogenesis is TNF-alpha dependent in a murine tooth extraction model. J. Bone Miner. Res. 2009, 24:1770-1781.
68. Van Wijngaarden P., Brereton H.M., Coster D.J., William K.A. Stability of housekeeping gene expression in the rat retina during exposure to cyclic hyperoxia. Mol. Vision 2007, 13:1508-1515.
69. Von Muhlen D., Safii S., Jassal S.K., Svartberg J., Barrett-Connor E. Associations between the metabolic syndrome and bone health in older men and women: the Rancho Bernardo Study. Osteoporos. Int. 2007, 18:1337-1344.
70. Wang J., Shang F., Jiang R., Liu L., Wang S., Hou J., Huan M., Mei Q. Nitric oxide-donating genistein prodrug: design, synthesis, and bioactivity on MC3T3-E1 cells. J. Pharmacol. Sci. 2007, 104:82-89.
71. Wauters M., Considine R.V., Van Gaal L.F. Human leptin: from an adipocyte hormone to an endocrine mediator. Eur. J. Endocrinol. 2000, 143:293-311.
72. Whyte M.P., Mahuren J.D., Fedde K.N., Cole F.S., McCabe E.R.B., Coburn S.P. Perinatal hypophosphatasia: tissue levels of vitamin B6 are unremarkable despite markedly increased circulating concentrations of pyridoxal-5'-phosphate. Evidence for an ectoenzyme role for tissue-nonspecific alkaline phosphatase. J. Clin. Invest. 1988, 81:1234-1239.
73. Yamaguchi T., Sugimoto T., Yano S., Yamauchi M., Sowa H., Chen Q., Chihara K. Plasma lipids and osteoporosis in postmenopausal women. Endocr. J. 2002, 49:211-217.
74. Yoshimura H., Muneta T., Nimura A., Yokoyama A., Koga H., Sekiya I. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res. 2007, 327:449-462.
75. Zhao M., Qiao M., Oyajobi B.O., Mundy G.R., Chen D. E3 ubiquitin ligase Smurf1 mediates core-binding factor alpha1/Runx2 degradation and plays a specific role in osteoblast differentiation. J. Biol. Chem. 2003, 278:27939-27944.
76. Zuk P.A., Zhu M., Huang J., Futrell J.W., Katz A.J., Benhaim P., Lorenz H.P., Hedrick M.H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001, 7:211-228.