The Phosphate Source Influences Gene Expression and Quality of Mineralization during In Vitro Osteogenic Differentiation of Human Mesenchymal Stem Cells

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Schäck, Luisa M ^a   Noack, Sandra ^a   Winkler, Ramona ^a   Wißmann, Gesa ^b   Behrens, Peter ^b   Wellmann, Mathias ^a   Jagodzinski, Michael ^a   Krettek, Christian ^a   Hoffmann, Andrea ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALCIUM PHOSPHATE; GLYCEROL 2 PHOSPHATE; ORGANOPHOSPHATE; PHOSPHATE; BIOLOGICAL MARKER;

ADULT; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; CELL DIFFERENTIATION; CHEMICAL COMPOSITION; COLORIMETRY; CONCENTRATION (PARAMETERS); FEMALE; GENE EXPRESSION; GENETIC MARKER; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INFRARED SPECTROSCOPY; MALE; MESENCHYMAL STEM CELL; OSTEOBLAST; X RAY DIFFRACTION; CYTOLOGY; MESENCHYMAL STROMA CELL; METABOLISM;

BIOMARKERS; CALCIFICATION, PHYSIOLOGIC; CELL DIFFERENTIATION; GENE EXPRESSION; HUMANS; IN VITRO TECHNIQUES; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; PHOSPHATES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; X-RAY DIFFRACTION;

EID: 84879142499     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065943     Document Type: Article

References (50)

1. Lian JB, Stein GS, (1993) The developmental stages of osteoblast growth and differentiation exhibit selective responses of genes to growth factors (TGF beta 1) and hormones (vitamin D and glucocorticoids). The Journal of Oral Implantology 19: 95-105.
2. Bieback K, Hecker A, Kocaömer A, Lannert H, Schallmoser K, et al. (2009) Human alternatives to fetal bovine serum for the expansion of mesenchymal stromal cells from bone marrow. Stem Cells 27: 2331-2341.
3. Tekkatte C, Gunasingh GP, Cherian KM, Sankaranarayanan K (2011) "Humanized" stem cell culture techniques: the animal serum controversy. Stem Cells International: 504723.
4. Sotiropoulou PA, Perez SA, Salagianni M, Baxevanis CN, Papamichail M, (2006) Cell culture medium composition and translational adult bone marrow-derived stem cell research. Stem Cells 24: 1409-1410.
5. Hamidouche Z, Haÿ E, Vaudin P, Charbord P, Schüle R, et al. (2008) FHL2 mediates dexamethasone-induced mesenchymal cell differentiation into osteoblasts by activating Wnt/beta-catenin signaling-dependent Runx2 expression. The FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 22: 3813-3822.
6. Jaiswal N, Haynesworth SE, Caplan AI, Bruder SP, (1997) Osteogenic differentiation of purified, culture-expanded human mesenchymal stem cells in vitro. Journal of Cellular Biochemistry 64: 295-312.
7. Lian JB, Stein GS, (1995) Development of the osteoblast phenotype: molecular mechanisms mediating osteoblast growth and differentiation. The Iowa Orthopaedic Journal 15: 118-140.
8. Chang P-L, Blair HC, Zhao X, Chien Y, Chen D, et al. (2006) Comparison of fetal and adult marrow stromal cells in osteogenesis with and without glucocorticoids. Connective Tissue Research 47: 67-76.
9. Beresford JN, Joyner CJ, Devlin C, Triffitt JT, (1994) The effects of dexamethasone and 1,25-dihydroxyvitamin D3 on osteogenic differentiation of human marrow stromal cells in vitro. Archives of Oral Biology 39: 941-947.
10. Cheng SL, (1994) Differentiation of human bone marrow osteogenic stromal cells in vitro: induction of the osteoblast phenotype by dexamethasone. Endocrinology 134: 277-286.
11. Pittenger MF, (2008) Mesenchymal stem cells from adult bone marrow. Methods in Molecular Biology (Clifton, NJ) 449: 27-44.
12. Chung CH, Golub EE, Forbes E, Tokuoka T, Shapiro IM, (1992) Mechanism of action of beta-glycerophosphate on bone cell mineralization. Calcified Tissue International 51: 305-311.
13. Miraoui H, Oudina K, Petite H, Tanimoto Y, Moriyama K, et al. (2009) Fibroblast growth factor receptor 2 promotes osteogenic differentiation in mesenchymal cells via ERK1/2 and protein kinase C signaling. The Journal of Biological Chemistry 284: 4897-4904.
14. Hamidouche Z, Fromigué O, Ringe J, Häupl T, Marie PJ, (2010) Crosstalks between integrin alpha 5 and IGF2/IGFBP2 signalling trigger human bone marrow-derived mesenchymal stromal osteogenic differentiation. BMC Cell Biology 11: 44.
15. Park KW, Waki H, Kim W-K, Davies BSJ, Young SG, et al. (2009) The small molecule phenamil induces osteoblast differentiation and mineralization. Molecular and Cellular Biology 29: 3905-3914.
16. Mathew S, Tustison KS, Sugatani T, Chaudhary LR, Rifas L, et al. (2008) The mechanism of phosphorus as a cardiovascular risk factor in CKD. Journal of the American Society of Nephrology 19: 1092-1105.
17. Quarles LD, Yohay DA, Lever LW, Caton R, Wenstrup RJ, (1992) Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: an in vitro model of osteoblast development. Journal of Bone and Mineral Research 7: 683-692.
18. Boskey AL, Roy R, (2008) Cell culture systems for studies of bone and tooth mineralization. Chemical Reviews 108: 4716-4733.
19. Hoemann CD, El-Gabalawy H, McKee MD, (2009) In vitro osteogenesis assays: influence of the primary cell source on alkaline phosphatase activity and mineralization. Pathologie-biologie 57: 318-323.
20. Hunter GK, Goldberg HA, (1994) Modulation of crystal formation by bone phosphoproteins: role of glutamic acid-rich sequences in the nucleation of hydroxyapatite by bone sialoprotein. The Biochemical Journal 302 Pt 1: 175-179.
21. Addison WN, Azari F, Sørensen ES, Kaartinen MT, McKee MD, (2007) Pyrophosphate inhibits mineralization of osteoblast cultures by binding to mineral, up-regulating osteopontin, and inhibiting alkaline phosphatase activity. The Journal of Biological Chemistry 282: 15872-15883.
22. Wolf G, (1996) Function of the bone protein osteocalcin: definitive evidence. Nutrition Reviews 54: 332-333.
23. Ali AT, Penny CB, Paiker JE, Psaras G, Ikram F, et al. (2006) The effect of alkaline phosphatase inhibitors on intracellular lipid accumulation in preadipocytes isolated from human mammary tissue. Annals of Clinical Biochemistry 43: 207-213.
24. Ichikawa H, Sugimoto T, (2002) The difference of osteocalcin-immunoreactive neurons in the rat dorsal root and trigeminal ganglia: co-expression with nociceptive transducers and central projection. Brain Research 958: 459-462.
25. Benayahu D, Shamay A, Wientroub S, (1997) Osteocalcin (BGP), gene expression, and protein production by marrow stromal adipocytes. Biochemical and Biophysical Research Communications 231: 442-446.
26. Foresta C, Strapazzon G, De Toni L, Gianesello L, Calcagno A, et al. (2010) Evidence for osteocalcin production by adipose tissue and its role in human metabolism. The Journal of Clinical Endocrinology and Metabolism 95: 3502-3506.
27. Thiede MA, Smock SL, Petersen DN, Grasser WA, Thompson DD, et al. (1994) Presence of messenger ribonucleic acid encoding osteocalcin, a marker of bone turnover, in bone marrow megakaryocytes and peripheral blood platelets. Endocrinology 135: 929-937.
28. Cassella JP, Garrington N, Stamp TC, Ali SY, (1995) An electron probe X-ray microanalytical study of bone mineral in osteogenesis imperfecta. Calcified Tissue International 56: 118-122.
29. Puchtler H, Meloan SN, Terry MS, (1969) On the history and mechanism of alizarin and alizarin red S stains for calcium. Journal of Histochemistry and Cytochemistry 17: 110.
30. Puchtler H, Meloan SN, (1978) Demonstration of phosphates in calcium deposits: A modification of von Kossa's reaction. Histochemistry 56: 177-185.
31. Mori K, Shioi A, Jono S, Nishizawa Y, Morii H, (1999) Dexamethasone Enhances In Vitro Vascular Calcification by Promoting Osteoblastic Differentiation of Vascular Smooth Muscle Cells. Arteriosclerosis, Thrombosis, and Vascular Biology 19: 2112-2118.
32. Mori K, Shioi A, Jono S, Nishizawa Y, Morii H, (1998) Expression of matrix Gla protein (MGP) in an in vitro model of vascular calcification. FEBS Letters 433: 19-22.
33. Proudfoot D, Skepper JN, Hegyi L, Bennett MR, Shanahan CM, et al. (2000) Apoptosis regulates human vascular calcification in vitro: evidence for initiation of vascular calcification by apoptotic bodies. Circulation Research 87: 1055-1062.
34. Shahab-Osterloh S, Witte F, Hoffmann A, Winkel A, Laggies S, et al. (2010) Mesenchymal stem cell-dependent formation of heterotopic tendon-bone insertions (osteotendinous junctions). Stem Cells 28: 1590-1601.
35. Stich S, Haag M, Häupl T, Sezer O, Notter M, et al. (2009) Gene expression profiling of human mesenchymal stem cells chemotactically induced with CXCL12. Cell and Tissue Research 336: 225-236.
36. Beck GR, Zerler B, Moran E, (2000) Phosphate is a specific signal for induction of osteopontin gene expression. Proceedings of the National Academy of Sciences of the United States of America 97: 8352-8357.
37. Beck GR, (2003) Inorganic phosphate as a signaling molecule in osteoblast differentiation. Journal of Cellular Biochemistry 90: 234-243.
38. Beck GR, Knecht N, (2003) Osteopontin regulation by inorganic phosphate is ERK1/2-, protein kinase C-, and proteasome-dependent. The Journal of Biological Chemistry 278: 41921-41929.
39. Paschalis EP, Mendelsohn R, Boskey AL, (2011) Infrared assessment of bone quality: a review. Clinical Orthopaedics and Related Research 469: 2170-2178.
40. Boskey AL, Gadaleta S, Gundberg C, Doty SB, Ducy P, et al. (1998) Fourier transform infrared microspectroscopic analysis of bones of osteocalcin-deficient mice provides insight into the function of osteocalcin. Bone 23: 187-196.
41. Paschalis EP, Verdelis K, Doty SB, Boskey AL, Mendelsohn R, et al. (2001) Spectroscopic characterization of collagen cross-links in bone. Journal of Bone and Mineral Research 16: 1821-1828.
42. Farlay D, Panczer G, Rey C, Delmas PD, Boivin G, (2010) Mineral maturity and crystallinity index are distinct characteristics of bone mineral. Journal of Bone and Mineral Metabolism 28: 433-445.
43. Fowler BO, Moreno EC, Brown WE, (1966) Infra-red spectra of hydroxyapatite, octacalcium phosphate and pyrolysed octacalcium phosphate. Archives of Oral Biology 11: 477-492.
44. Lynch MP, Capparelli C, Stein JL, Stein GS, Lian JB, (1998) Apoptosis during bone-like tissue development in vitro. Journal of Cellular Biochemistry 68: 31-49.
45. Tenenbaum HC, Heersche JNM, (1982) Differentiation of osteoblasts and formation of mineralized bone in vitro. Calcified Tissue International 34: 76-79.
46. Khoshniat S, Bourgine A, Julien M, Petit M, Pilet P, et al. (2011) Phosphate-dependent stimulation of MGP and OPN expression in osteoblasts via the ERK1/2 pathway is modulated by calcium. Bone 48: 894-902.
47. Julien M, Khoshniat S, Lacreusette A, Gatius M, Bozec A, et al. (2009) Phosphate-dependent regulation of MGP in osteoblasts: role of ERK1/2 and Fra-1. Journal of Bone and Mineral Research 24: 1856-1868.
48. Boskey AL, (1989) Hydroxyapatite formation in a dynamic collagen gel system: effects of type I collagen, lipids, and proteoglycans. The Journal of Physical Chemistry 93: 1628-1633.
49. Bonewald LF, Harris SE, Rosser J, Dallas MR, Dallas SL, et al. (2003) von Kossa staining alone is not sufficient to confirm that mineralization in vitro represents bone formation. Calcified Tissue International 72: 537-547.
50. Markovic M, Fowler B, Tung M, (2004) Preparation and comprehensive characterization of a calcium hydroxyapatite reference material. Journal of Research of the National Institute of Standards and Technology 109: 553-568.