Calcium phosphate-bearing matrices induce osteogenic differentiation of stem cells through adenosine signaling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 3, 2014, Pages 990-995

  Shih, Yu Ru V ^a,b,c   Hwang, Yongsung ^a   Phadke, Ameya ^a   Kang, Heemin ^a,d   Hwang, Nathaniel S ^e   Caro, Eduardo J ^d   Nguyen, Steven ^d   Siu, Michael ^a   Theodorakis, Emmanuel A ^d   Gianneschi, Nathan C ^d   Vecchio, Kenneth S ^f   Chien, Shu ^a,b,f   Lee, Oscar K ^c,g   Varghese, Shyni ^a,b,d,f  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Seoul National University   (South Korea)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^g TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

Biomimetic material; Bone metabolism; Mineralized matrix; Phosphate signaling

Indexed keywords

ADENOSINE; ADENOSINE A2B RECEPTOR; ADENOSINE TRIPHOSPHATE; CALCIUM PHOSPHATE; PHOSPHATE TRANSPORTER; SOLUTE CARRIER FAMILY 20A1; UNCLASSIFIED DRUG;

ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; OSTEOBLAST; PHOSPHATE METABOLISM; PHOSPHATE TRANSPORT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

BIOMIMETIC MATERIAL; BONE METABOLISM; MINERALIZED MATRIX; PHOSPHATE SIGNALING;

ADENOSINE; ADENOSINE TRIPHOSPHATE; BIOCOMPATIBLE MATERIALS; BONE AND BONES; CALCIUM PHOSPHATES; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; PHENOTYPE; PHOSPHATES; RECEPTOR, ADENOSINE A2B; REGENERATION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SODIUM-PHOSPHATE COTRANSPORTER PROTEINS, TYPE III; STEM CELLS;

EID: 84892925815     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321717111     Document Type: Article

References (58)

1. Hwang Y, Phadke A, Varghese S (2011) Engineered microenvironments for selfrenewal and musculoskeletal differentiation of stem cells. Regen Med 6(4):505-524.
2. Burdick JA, Vunjak-Novakovic G (2009) Engineered microenvironments for controlled stem cell differentiation. Tissue Eng Part A 15(2):205-219.
3. Lutolf MP, et al. (2003) Repair of bone defects using synthetic mimetics of collagenous extracellular matrices. Nat Biotechnol 21(5):513-518.
4. Ayala R, et al. (2011) Engineering the cell-material interface for controlling stem cell adhesion, migration, and differentiation. Biomaterials 32(15):3700-3711.
5. Benoit DS, Schwartz MP, Durney AR, Anseth KS (2008) Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat Mater 7(10):816-823.
6. Dalby MJ, et al. (2007) The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6(12):997-1003.
7. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677-689.
8. Huebsch N, et al. (2010) Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater 9(6):518-526.
9. Datta N, et al. (2006) In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc Natl Acad Sci USA 103(8):2488-2493.
10. Phadke A, et al. (2013) Effect of scaffold microarchitecture on osteogenic differentiation of human mesenchymal stem cells. Eur Cell Mater 25:114-128, discussion 128-129.
11. Phadke A, Shih YR, Varghese S (2012) Mineralized synthetic matrices as an instructive microenvironment for osteogenic differentiation of human mesenchymal stem cells. Macromol Biosci 12(8):1022-1032.
12. Bhumiratana S, et al. (2011) Nucleation and growth of mineralized bone matrix on silk-hydroxyapatite composite scaffolds. Biomaterials 32(11):2812-2820.
13. Yuan H, et al. (2010) Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proc Natl Acad Sci USA 107(31):13614-13619.
14. Roberts SJ, et al. (2011) The combined bone forming capacity of human periosteal derived cells and calcium phosphates. Biomaterials 32(19):4393-4405.
15. Johal HS, Buckley RE, Le IL, Leighton RK (2009) A prospective randomized controlled trial of a bioresorbable calcium phosphate paste (alpha-BSM) in treatment of displaced intra-articular calcaneal fractures. J Trauma 67(4):875-882.
16. Vaquette C, Ivanovski S, Hamlet SM, Hutmacher DW (2013) Effect of culture conditions and calcium phosphate coating on ectopic bone formation. Biomaterials 34(22):5538-5551.
17. Choi S, Murphy WL (2013) A screening approach reveals the influence of mineral coating morphology on human mesenchymal stem cell differentiation. Biotechnol J 8(4):496-501.
18. Chai YC, Roberts SJ, Schrooten J, Luyten FP (2011) Probing the osteoinductive effect of calcium phosphate by using an in vitro biomimetic model. Tissue Eng Part A 17(7-8):1083-1097.
19. Chou YF, Huang W, Dunn JC, Miller TA, Wu BM (2005) The effect of biomimetic apatite structure on osteoblast viability, proliferation, and gene expression. Biomaterials 26(3):285-295.
20. Cowan CM, et al. (2004) Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 22(5):560-567.
21. Hoppe A, Güldal NS, Boccaccini AR (2011) A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials 32(11):2757-2774.
22. Autefage H, et al. (2009) Adsorption and release of BMP-2 on nanocrystalline apatitecoated and uncoated hydroxyapatite/beta-tricalcium phosphate porous ceramics. J Biomed Mater Res B Appl Biomater 91(2):706-715.
23. Lee JS, Suarez-Gonzalez D, Murphy WL (2011) Mineral coatings for temporally controlled delivery of multiple proteins. Adv Mater 23(37):4279-4284.
24. Chai YC, et al. (2012) Mechanisms of ectopic bone formation by human osteoprogenitor cells on CaP biomaterial carriers. Biomaterials 33(11):3127-3142.
25. Barradas AM, et al. (2012) A calcium-induced signaling cascade leading to osteogenic differentiation of human bone marrow-derived mesenchymal stromal cells. Biomaterials 33(11):3205-3215.
26. Beck GR, Jr. (2003) Inorganic phosphate as a signaling molecule in osteoblast differentiation. J Cell Biochem 90(2):234-243.
27. Beck GR, Jr., Zerler B, Moran E (2000) Phosphate is a specific signal for induction of osteopontin gene expression. Proc Natl Acad Sci USA 97(15):8352-8357.
28. Wen L, et al. (2012) L-type calcium channels play a crucial role in the proliferation and osteogenic differentiation of bone marrow mesenchymal stem cells. Biochem Biophys Res Commun 424(3):439-445.
29. Yadav MC, et al. (2011) Loss of skeletal mineralization by the simultaneous ablation of PHOSPHO1 and alkaline phosphatase function: A unified model of the mechanisms of initiation of skeletal calcification. J Bone Miner Res 26(2):286-297.
30. Huitema LF, et al. (2012) Entpd5 is essential for skeletal mineralization and regulates phosphate homeostasis in zebrafish. Proc Natl Acad Sci USA 109(52):21372-21377.
31. Jono S, et al. (2000) Phosphate regulation of vascular smooth muscle cell calcification. Circ Res 87(7):E10-E17.
32. Giachelli CM, et al. (2001) Vascular calcification and inorganic phosphate. Am J Kidney Dis 38(4, Suppl 1):S34-S37.
33. Yoshiko Y, Candeliere GA, Maeda N, Aubin JE (2007) Osteoblast autonomous Pi regulation via Pit1 plays a role in bone mineralization. Mol Cell Biol 27(12):4465-4474.
34. Li X, Giachelli CM (2007) Sodium-dependent phosphate cotransporters and vascular calcification. Curr Opin Nephrol Hypertens 16(4):325-328.
35. Phadke A, Zhang C, Hwang Y, Vecchio K, Varghese S (2010) Templated mineralization of synthetic hydrogels for bone-like composite materials: Role of matrix hydrophobicity. Biomacromolecules 11(8):2060-2068.
36. Raynaud S, Champion E, Bernache-Assollant D, Thomas P (2002) Calcium phosphate apatites with variable Ca/P atomic ratio I. Synthesis, characterisation and thermal stability of powders. Biomaterials 23(4):1065-1072.
37. Novak I (2003) ATP as a signaling molecule: The exocrine focus. News Physiol Sci 18:12-17.
38. Nakano Y, Addison WN, Kaartinen MT (2007) ATP-mediated mineralization of MC3T3-E1 osteoblast cultures. Bone 41(4):549-561.
39. Zippel N, et al. (2012) Purinergic receptors influence the differentiation of human mesenchymal stem cells. Stem Cells Dev 21(6):884-900.
40. Alsberg E, et al. (2003) Regulating bone formation via controlled scaffold degradation. J Dent Res 82(11):903-908.
41. Boyer PD (1997) The ATP synthase-A splendid molecular machine. Annu Rev Biochem 66:717-749.
42. Bose S, French S, Evans FJ, Joubert F, Balaban RS (2003) Metabolic network control of oxidative phosphorylation: Multiple roles of inorganic phosphate. J Biol Chem 278(40):39155-39165.
43. Sugita A, et al. (2011) Cellular ATP synthesis mediated by type III sodium-dependent phosphate transporter Pit-1 is critical to chondrogenesis. J Biol Chem 286(4):3094-3103.
44. Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH (2008) Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 26(4):960-968.
45. Hoebertz A, Mahendran S, Burnstock G, Arnett TR (2002) ATP and UTP at low concentrations strongly inhibit bone formation by osteoblasts: A novel role for the P2Y2 receptor in bone remodeling. J Cell Biochem 86(3):413-419.
46. Orriss IR, et al. (2012) The regulation of osteoblast function and bone mineralisation by extracellular nucleotides: The role of p2x receptors. Bone 51(3):389-400.
47. Zimmermann H (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch Pharmacol 362(4-5):299-309.
48. Costa MA, et al. (2011) On the role of subtype selective adenosine receptor agonists during proliferation and osteogenic differentiation of human primary bone marrow stromal cells. J Cell Physiol 226(5):1353-1366.
49. Carroll SH, et al. (2012) A2B adenosine receptor promotes mesenchymal stem cell differentiation to osteoblasts and bone formation in vivo. J Biol Chem 287(19):15718-15727.
50. Gharibi B, Abraham AA, Ham J, Evans BA (2011) Adenosine receptor subtype expression and activation influence the differentiation of mesenchymal stem cells to osteoblasts and adipocytes. J Bone Miner Res 26(9):2112-2124.
51. He W, Mazumder A, Wilder T, Cronstein BN (2013) Adenosine regulates bone metabolism via A1, A2A, and A2B receptors in bone marrow cells from normal humans and patients with multiple myeloma. FASEB J 27(9):3446-3454.
52. Khoshniat S, et al. (2011) Phosphate-dependent stimulation of MGP and OPN expression in osteoblasts via the ERK1/2 pathway is modulated by calcium. Bone 48(4):894-902.
53. Suzuki A, et al. (2006) Enhanced expression of the inorganic phosphate transporter Pit-1 is involved in BMP-2-induced matrix mineralization in osteoblast-like cells. J Bone Miner Res 21(5):674-683.
54. Li X, Yang HY, Giachelli CM (2006) Role of the sodium-dependent phosphate cotransporter, Pit-1, in vascular smooth muscle cell calcification. Circ Res 98(7):905-912.
55. Cowan CM, et al. (2012) NELL-1 increases pre-osteoblast mineralization using both phosphate transporter Pit1 and Pit2. Biochem Biophys Res Commun 422(3):351-357.
56. Nakade O, Takahashi K, Takuma T, Aoki T, Kaku T (2001) Effect of extracellular calcium on the gene expression of bone morphogenetic protein-2 and -4 of normal human bone cells. J Bone Miner Metab 19(1):13-19.
57. Wang N, et al. (2012) Reduced bone turnover in mice lacking the P2Y (13) receptor of ADP. Mol Endocrinol 26(1):142-152.
58. Gartland A, et al. (2012) Polymorphisms in the P2X7 receptor gene are associated with low lumbar spine bone mineral density and accelerated bone loss in post-menopausal women. Eur J Hum Genet 20(5):559-564.