Nano-hydroxyapatite modulates osteoblast lineage commitment by stimulation of DNA methylation and regulation of gene expression

Biomaterials

Volumn 65, Issue , 2015, Pages 32-42

  Ha, Shin Woo ^b   Jang, Hae Lin ^c   Nam, Ki Tae ^c   Beck, George R ^a,b  

^a ATLANTA VA MEDICAL CENTER   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Seoul National University   (South Korea)

Author keywords

Alkaline phosphatase; Gene expression; Hydroxyapatite; Nanoparticle; Osteoblast; Osteogenesis

Indexed keywords

ALKYLATION; CELLS; CYTOLOGY; DENTAL PROSTHESES; GENE EXPRESSION; GENES; HYDROXYAPATITE; METHYLATION; NANOCOMPOSITES; NANOPARTICLES; OSTEOBLASTS; PHOSPHATASES; SCAFFOLDS (BIOLOGY);

ALKALINE PHOSPHATASE; BIOLOGICAL CONDITIONS; BIOLOGICAL EFFECTS; DENTAL APPLICATIONS; EPIGENETIC REGULATION; NANO-HYDROXYAPATITE; OSTEOGENESIS; STRUCTURAL COMPONENT;

GENE EXPRESSION REGULATION;

ALKALINE PHOSPHATASE; CALCIUM OXIDE; HYDROXYAPATITE; NANOHYDROXYAPATITE; NANOMATERIAL; SILICA NANOPARTICLE; UNCLASSIFIED DRUG; BIOMATERIAL;

ANIMAL CELL; ARTICLE; BIOLOGICAL ACTIVITY; BONE MARROW STROMA CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINEAGE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DNA METHYLATION; ELECTRON DIFFRACTION; EPIGENETICS; EXPOSURE; GENE EXPRESSION REGULATION; MOUSE; NANOFABRICATION; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; TRANSMISSION ELECTRON MICROSCOPY; X RAY POWDER DIFFRACTION; ANIMAL; BONE DEVELOPMENT; CELL LINE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; MESENCHYMAL STROMA CELL; ULTRASTRUCTURE;

ALKALINE PHOSPHATASE; ANIMALS; BIOCOMPATIBLE MATERIALS; CELL DIFFERENTIATION; CELL LINE; DNA METHYLATION; DURAPATITE; EPIGENESIS, GENETIC; MESENCHYMAL STROMAL CELLS; MICE; NANOSTRUCTURES; OSTEOBLASTS; OSTEOGENESIS; PROMOTER REGIONS, GENETIC;

EID: 84937509858     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.06.039     Document Type: Article

References (78)

1. Palmer L.C., Newcomb C.J., Kaltz S.R., Spoerke E.D., Stupp S.I. Biomimetic systems for hydroxyapatite mineralization inspired by bone and enamel. Chem. Rev. 2008, 108:4754-4783.
2. Bohner M., Tadier S., van Garderen N., de Gasparo A., Dobelin N., Baroud G. Synthesis of spherical calcium phosphate particles for dental and orthopedic applications. Biomatter 2013, 3. e25103-1-15.
3. Hunter L.W., Charlesworth J.E., Yu S., Lieske J.C., Miller V.M. Calcifying nanoparticles promote mineralization in vascular smooth muscle cells: implications for atherosclerosis. Int. J. Nanomed. 2014, 9:2689-2698.
4. Dai X.Y., Zhao M.M., Cai Y., Guan Q.C., Zhao Y., Guan Y., Kong W., Zhu W.G., Xu M.J., Wang X. Phosphate-induced autophagy counteracts vascular calcification by reducing matrix vesicle release. Kidney Int. 2013, 83:1042-1051.
5. Shanahan C.M., Crouthamel M.H., Kapustin A., Giachelli C.M. Arterial calcification in chronic kidney disease: key roles for calcium and phosphate. Circ. Res. 2011, 109:697-711.
6. Kirsch T., Nah H.D., Shapiro I.M., Pacifici M. Regulated production of mineralization-competent matrix vesicles in hypertrophic chondrocytes. J.Cell Biol. 1997, 137:1149-1160.
7. Belem L.C., Zanetti G., Souza A.S., Hochhegger B., Guimaraes M.D., Nobre L.F., Rodrigues R.S., Marchiori E. Metastatic pulmonary calcification: state-of-the-art review focused on imaging findings. Respir. Med. 2014, 108:668-676.
8. Wu L.N., Genge B.R., Dunkelberger D.G., LeGeros R.Z., Concannon B., Wuthier R.E. Physicochemical characterization of the nucleational core of matrix vesicles. J.Biol. Chem. 1997, 272:4404-4411.
9. Bertazzo S., Gentleman E., Cloyd K.L., Chester A.H., Yacoub M.H., Stevens M.M. Nano-analytical electron microscopy reveals fundamental insights into human cardiovascular tissue calcification. Nat. Mater. 2013, 12:576-583.
10. Reynolds J.L., Joannides A.J., Skepper J.N., McNair R., Schurgers L.J., Proudfoot D., Jahnen-Dechent W., Weissberg P.L., Shanahan C.M. Human vascular smooth muscle cells undergo vesicle-mediated calcification in response to changes in extracellular calcium and phosphate concentrations: a potential mechanism for accelerated vascular calcification in ESRD. J.Am. Soc. Nephrol. 2004, 15:2857-2867.
11. Lee S.Y., Kim H.Y., Gu S.W., Kim H.J., Yang D.H. 25-Hydroxyvitamin D levels and vascular calcification in predialysis and dialysis patients with chronic kidney disease. Kidney Blood Press Res. 2012, 35:349-354.
12. Villa-Bellosta R., Millan A., Sorribas V. Role of calcium-phosphate deposition in vascular smooth muscle cell calcification. Am. J. Physiol. Cell Physiol. 2011, 300:C210-C220.
13. Dalinka M.K., Melchior E.L. Soft tissue calcifications in systemic disease. Bull. N. Y. Acad. Med. 1980, 56:539-563.
14. Tanabe H., Akashi T., Kawachi H., Andou N., Eishi Y., Takizawa T., Koike M., Ichinose S. Identification of hydroxyapatite deposits in the smooth muscle cells and ganglion cells of autopsied small intestines. J.Med. Dent. Sci. 2004, 51:129-138.
15. Anderson H.C., Garimella R., Tague S.E. The role of matrix vesicles in growth plate development and biomineralization. Front. Biosci. 2005, 10:822-837.
16. Xiao Z., Camalier C.E., Nagashima K., Chan K.C., Lucas D.A., de la Cruz M.J., Gignac M., Lockett S., Issaq H.J., Veenstra T.D., Conrads T.P., Beck G.R. Analysis of the extracellular matrix vesicle proteome in mineralizing osteoblasts. J.Cell Physiol. 2007, 210:325-335.
17. Bonewald L.F. The amazing osteocyte. J.Bone Miner. Res. 2011, 26:229-238.
18. Beck G.R. Inorganic phosphate as a signaling molecule in osteoblast differentiation. J.Cell Biochem. 2003, 90:234-243.
19. Aubin J.E. Regulation of osteoblast formation and function. Rev. Endocr. Metab. Disord. 2001, 2:81-94.
20. Beck G.R., Sullivan E.C., Moran E., Zerler B. Relationship between alkaline phosphatase levels, osteopontin expression, and mineralization in differentiating MC3T3-E1 osteoblasts. J.Cell Biochem. 1998, 68:269-280.
21. Beck G.R., Moran E., Knecht N. Inorganic phosphate regulates multiple genes during osteoblast differentiation, including Nrf2. Exp. Cell Res. 2003, 288:288-300.
22. Conrads K.A., Yi M., Simpson K.A., Lucas D.A., Camalier C.E., Yu L.R., Veenstra T.D., Stephens R.M., Conrads T.P., Beck G.R. Acombined proteome and microarray investigation of inorganic phosphate-induced pre-osteoblast cells. Mol. Cell. Proteomics 2005, 4:1284-1296.
23. Whyte M.P. Hypophosphatasia and the role of alkaline phosphatase in skeletal mineralization. Endocr. Rev. 1994, 15:439-461.
24. Rathburn J.C. Hypophosphatasia, a new developmental anomaly. Am. J. Dis. Child. 1948, 75:822-831.
25. Fedde K.N., Blair L., Silverstein J., Coburn S.P., Ryan L.M., Weinstein R.S., Waymire K., Narisawa S., Millan J.L., MacGregor G.R., Whyte M.P. Alkaline phosphatase knock-out mice recapitulate the metabolic and skeletal defects of infantile hypophosphatasia. J.Bone Miner. Res. 1999, 14:2015-2026.
26. Collas P. Epigenetic states in stem cells. Biochim. Biophys. Acta 2009, 1790:900-905.
27. Delgado-Calle J., Sanudo C., Sanchez-Verde L., Garcia-Renedo R.J., Arozamena J., Riancho J.A. Epigenetic regulation of alkaline phosphatase in human cells of the osteoblastic lineage. Bone 2011, 49:830-838.
28. Escalante-Alcalde D., Recillas-Targa F., Hernandez-Garcia D., Castro-Obregon S., Terao M., Garattini E., Covarrubias L. Retinoic acid and methylation Cis-regulatory elements control the mouse tissue non-specific alkaline phosphatase gene expression. Mech. Dev. 1996, 57:21-32.
29. Cho Y.D., Yoon W.J., Kim W.J., Woo K.M., Baek J.H., Lee G., Ku Y., van Wijnen A.J., Ryoo H.M. Epigenetic modifications and canonical wingless/Int-1 class (Wnt) signaling enable trans-differentiation of nonosteogenic cells into osteoblasts. J.Biol. Chem. 2014, 289:20120-20128.
30. Stoccoro A., Karlsson H.L., Coppede F., Migliore L. Epigenetic effects of nano-sized materials. Toxicology 2013, 313:3-14.
31. Furuzono T., Yasuda S., Kimura T., Kyotani S., Tanaka J., Kishida A. Nano-scaled hydroxyapatite/polymer composite Iv. Fabrication and cell adhesion properties of a three-dimensional scaffold made of composite material with a silk fibroin substrate to develop a percutaneous device. J.Artif. Organs 2004, 7:137-144.
32. Ito Y., Tanaka N., Fujimoto Y., Yasunaga Y., Ishida O., Agung M., Ochi M. bone formation using novel interconnected porous calcium hydroxyapatite ceramic hybridized with cultured marrow stromal stem cells derived from green rat. J.Biomed. Mater. Res. A 2004, 69:454-461.
33. Itoh S., Kikuchi M., Koyama Y., Takakuda K., Shinomiya K., Tanaka J. Development of a hydroxyapatite/collagen nanocomposite as a medical device. Cell Transpl. 2004, 13:451-461.
34. Sun D., Chen Y., Tran R.T., Xu S., Xie D., Jia C., Wang Y., Guo Y., Zhang Z., Guo J., Yang J., Jin D., Bai X. Citric acid-based hydroxyapatite composite scaffolds enhance calvarial regeneration. Sci. Rep. 2014, 4:6912.
35. Li L., Pan H.H., Tao J.H., Xu X.R., Mao C.Y., Gu X.H., Tang R.K. Repair of enamel by using hydroxyapatite nanoparticles as the building blocks. J.Mater. Chem. 2008, 18:4079-4084.
36. Zhou H., Lee J. Nanoscale hydroxyapatite particles for bone tissue engineering. Acta Biomater. 2011, 7:2769-2781.
37. Zhang J.Z., Liu G.Y., Wu Q.O., Zuo J.L., Qin Y.G., Wang J.C. Novel mesoporous hydroxyapatite/chitosan composite for bone repair. J.Bionic Eng. 2012, 9:243-251.
38. Park J.W., Suh J.Y., Chung H.J. Effects of calcium ion incorporation on osteoblast gene expression in MC3T3-E1 cells cultured on microstructured titanium surfaces. J.Biomed. Mater. Res. A 2008, 86:117-126.
39. Noor Z. Nanohydroxyapatite application to osteoporosis management. J.Osteoporos. 2013, 679025:1-6.
40. Nandi S.K., Roy S., Mukherjee P., Kundu B., De D.K., Basu D. Orthopaedic applications of bone graft & graft substitutes: a review. Indian J. Med. Res. 2010, 132:15-30.
41. Ha S.W., Weitzmann M.N., Beck G.R. Bioactive silica nanoparticles promote osteoblast differentiation through stimulation of autophagy and direct association with LC3 and p62. ACS Nano 2014, 8:5898-5910.
42. Camalier C.E., Yi M., Yu L.R., Hood B.L., Conrads K.A., Lee Y.J., Lin Y., Garneys L.M., Bouloux G.F., Young M.R., Veenstra T.D., Stephens R.M., Colburn N.H., Conrads T.P., Beck G.R. An integrated understanding of the physiological response to elevated extracellular phosphate. J.Cell Physiol. 2013, 228:1536-1550.
43. Aubin J.E., Triffitt J.T. Mesenchymal Stem Cells and Osteoblast Differentiation 2002, Academic Press, San Diego. second ed.
44. Sudo H., Kodama H.A., Amagai Y., Yamamoto S., Kasai S. Invitro differentiation and calcification in a new clonal osteogenic cell line derived from newborn mouse calvaria. J.Cell Biol. 1983, 96:191-198.
45. Bonewald L.F. Establishment and characterization of an osteocyte-like cell line, MLO-Y4. J.Bone Miner. Metab. 1999, 17:61-65.
46. Beck G.R., Zerler B., Moran E. Phosphate is a specific signal for induction of osteopontin gene expression. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:8352-8357.
47. Stöber W., Fink A., Bohn E. Controlled growth of monodisperse silica spheres in the micron size range. J.Colloid Interf. Sci. 1968, 62-69.
48. Beck G.R., Ha S.W., Camalier C.E., Yamaguchi M., Li Y., Lee J.K., Weitzmann M.N. Bioactive silica-based nanoparticles stimulate bone-forming osteoblasts, suppress bone-resorbing osteoclasts, and enhance bone mineral density invivo. Nanomedicine 2012, 8:793-803.
49. Rosser J., Bonewald L.F. Studying osteocyte function using the cell lines MLO-Y4 and MLO-A5. Methods Mol. Biol. 2012, 816:67-81.
50. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative Pcr and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
51. Hashimoto K., Kokubun S., Itoi E., Roach H.I. Improved quantification of DNA methylation using methylation-sensitive restriction enzymes and real-time Pcr. Epigenetics 2007, 2:86-91.
52. Ha S.W., Camalier C.E., Beck G.R., Lee J.K. New method to prepare very stable and biocompatible fluorescent silica nanoparticles. Chem. Commun. (Camb) 2009, 2881-2883.
53. Miranda T.B., Jones P.A. DNA methylation: the nuts and bolts of repression. J.Cell Physiol. 2007, 213:384-390.
54. Delgado-Calle J., Arozamena J., Perez-Lopez J., Bolado-Carrancio A., Sanudo C., Agudo G., de la Vega R., Alonso M.A., Rodriguez-Rey J.C., Riancho J.A. Role of Bmps in the regulation of sclerostin as revealed by an epigenetic modifier of human bone cells. Mol. Cell Endocrinol. 2013, 369:27-34.
55. Vaes B.L., Lute C., van der Woning S.P., Piek E., Vermeer J., Blom H.J., Mathers J.C., Muller M., de Groot L.C., Steegenga W.T. Inhibition of methylation decreases osteoblast differentiation via a non-DNA-dependent methylation mechanism. Bone 2010, 46:514-523.
56. Jokerst J.V., Lobovkina T., Zare R.N., Gambhir S.S. Nanoparticle pegylation for imaging and therapy. Nanomedicine 2011, 6:715-728.
57. Borum L., Wilson O.C. surface modification of hydroxyapatite. Part II. silica. Biomaterials 2003, 24:3681-3688.
58. Choi H.W., Lee H.J., Kim K.J., Kim H.M., Lee S.C. Surface modification of hydroxyapatite nanocrystals by grafting polymers containing phosphonic acid groups. J.Colloid Interf. Sci. 2006, 304:277-281.
59. Tanaka H., Futaoka M., Hino R. Surface modification of calcium hydroxyapatite with pyrophosphoric acid. J.Colloid Interf. Sci. 2004, 269:358-363.
60. Koerten H.K., van der Meulen J. Degradation of calcium phosphate ceramics. J.Biomed. Mater. Res. 1999, 44:78-86.
61. Chow L.C. Next generation calcium phosphate-based biomaterials. Dent. Mater. J. 2009, 28:1-10.
62. Farbod K., Nejadnik M.R., Jansen J.A., Leeuwenburgh S.C. Interactions between inorganic and organic phases in bone tissue as a source of inspiration for design of novel nanocomposites. Tissue Eng. Part B Rev. 2014, 20:173-188.
63. Ha S.W., Sikorski J.A., Weitzmann M.N., Beck G.R. Bio-active engineered 50nm silica nanoparticles with bone anabolic activity: therapeutic index, effective concentration, and cytotoxicity profile invitro. Toxicol InVitro 2013, 28:354-364.
64. Beck G.R., Knecht N. Osteopontin regulation by inorganic phosphate is Erk1/2-, protein kinase C-, and proteasome-dependent. J.Biol. Chem. 2003, 278:41921-41929.
65. Camalier C.E., Young M.R., Bobe G., Perella C.M., Colburn N.H., Beck G.R. Elevated phosphate activates N-Ras and promotes cell transformation and skin tumorigenesis. Cancer Prev. Res. (Phila) 2010, 3:359-370.
66. Pasch A., Farese S., Graber S., Wald J., Richtering W., Floege J., Jahnen-Dechent W. Nanoparticle-based test measures overall propensity for calcification in serum. J.Am. Soc. Nephrol. 2012, 23:1744-1752.
67. Stein G.S., Zaidi S.K., Stein J.L., Lian J.B., van Wijnen A.J., Montecino M., Young D.W., Javed A., Pratap J., Choi J.Y., Ali S.A., Pande S., Hassan M.Q. Transcription-factor-mediated epigenetic control of cell fate and lineage commitment. Biochem. Cell Biol. 2009, 87:1-6.
68. Cheng X.D., Hashimoto H., Horton J.R., Zhang X. Mechanisms of DNA Methylation, Methyl-Cpg Recognition, and Demethylation in Mammals. Handbook of Epigenetics: the New Molecular and Medical Genetics 2011, 9-24.
69. Jeltsch A., Jurkowska R.Z. New concepts in DNA methylation. Trends Biochem. Sci. 2014, 39:310-318.
70. Buttitta L.A., Edgar B.A. Mechanisms controlling cell cycle exit upon terminal differentiation. Curr. Opin. Cell. Biol. 2007, 19:697-704.
71. Hunter G.K. Role of osteopontin in modulation of hydroxyapatite formation. Calcif. Tissue Int. 2013, 93:348-354.
72. Steitz S.A., Speer M.Y., McKee M.D., Liaw L., Almeida M., Yang H., Giachelli C.M. Osteopontin inhibits mineral deposition and promotes regression of ectopic calcification. Am. J. Pathol. 2002, 161:2035-2046.
73. Boskey A.L., Maresca M., Ullrich W., Doty S.B., Butler W.T., Prince C.W. Osteopontin-hydroxyapatite interactions invitro: inhibition of hydroxyapatite formation and growth in a gelatin-gel. Bone Miner. 1993, 22:147-159.
74. Block G.A., Hulbert-Shearon T.E., Levin N.W., Port F.K. Association of serum phosphorus and calcium X phosphate product with mortality risk in chronic hemodialysis patients: a national study. Am. J. Kidney Dis. 1998, 31:607-617.
75. Ketteler M., Schlieper G., Floege J. Calcification and cardiovascular health: new insights into an old phenomenon. Hypertension 2006, 47:1027-1034.
76. Jono S., McKee M.D., Murry C.E., Shioi A., Nishizawa Y., Mori K., Morii H., Giachelli C.M. Phosphate regulation of vascular smooth muscle cell calcification. Circ. Res. 2000, 87:E10-E17.
77. Garcia G.M., McCord G.C., Kumar R. Hydroxyapatite crystal deposition disease. Semin. Musculoskelet. Radiol. 2003, 7:187-193.
78. Clarke B. Normal bone anatomy and physiology. Clin. J. Am. Soc. Nephrol. 2008, 3(Suppl.3):S131-S139.