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Current Nanomedicine

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ISSN (Print): 2468-1873
ISSN (Online): 2468-1881

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Research Article

Nanoplatforms for Promoting Osteogenesis in Ovariectomy-Induced Osteoporosis in the Experimental Model

Author(s): Enas A. Fouad-Elhady, Hadeer A. Aglan*, Rasha E. Hassan, Gilane M. Sabry and Hanaa H. Ahmed

Volume 12, Issue 1, 2022

Published on: 11 April, 2022

Page: [44 - 62] Pages: 19

DOI: 10.2174/2468187312666220217104650

Price: $65

Abstract

Background: Osteoporosis is a debilitating bone ailment characterized by the obvious loss of bone mass and bone microarchitecture impairment.

Objective: This study aimed to illuminate the in vivo usefulness of nanotechnology as a treatment for osteoporosis via analyzing the effectiveness of nano-hydroxyapatite (nHa), nano-hydroxyapatite/ chitosan (nHa/C), and nano-hydroxyapatite/silver (nHa/S) in mitigation of osteoporosis in ovariectomized rats.

Methods: The characterization of the nHa, nHa/C, and nHa/S was carried out using TEM, SEM, FTIR, and Zeta potential measurements. This in vivo study included 48 adult female rats that were randomized into six groups (8 rats/group): (1) Sham-operated control, (2) osteoporotic, (3) nHa, (4) nHa/C, (5) nHa/S, and (6) Fosamax®. Serum osterix level was quantified using ELISA. Femur bone morphogenetic protein 2 and SMAD1 mRNA levels were evaluated by qPCR. The femur bones were scanned by DEXA for measurement of bone mineral density and bone mineral content. In addition, a histopathological examination of femur bones was performed.

Results: The present approach denoted that the treatment with nHa, nHa/C, or nHa/S yields a significant rise in serum level of osterix and mRNA levels of bone morphogenetic protein 2 and SMAD1 as well as significant enhancements of bone tissue minerals.

Conclusion: The findings affirmed the potency of nHa, nHa/C, and nHa/S as auspicious nanoplatforms for repairing bone defects in the osteoporotic rat model. The positive effect of the inspected nanoformulations arose from bone formation indicators in serum and tissue, and additionally, the reinforcement of bone density and content, which were verified by the histopathological description of bone tissue sections.

Keywords: Silver nanoparticle, nanohydroxyapatite, chitosan nanoplatform, bone formation, osteoporosis, rats, calcitonin.

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[1]
Sun X, Wei J, Lyu J, et al. Bone-targeting drug delivery system of biomineral-binding liposomes loaded with icariin enhances the treatment for osteoporosis. J Nanobiotechnology 2019; 17(1): 10.
[http://dx.doi.org/10.1186/s12951-019-0447-5] [PMID: 30670021]
[2]
Kauschke V, Hessland FM, Vehlow D, Müller M, Heiss C, Lips KS. High concentrations of polyelectrolyte complex nanoparticles decrease activity of osteoclasts. Molecules 2019; 24(12): 2346.
[http://dx.doi.org/10.3390/molecules24122346] [PMID: 31242715]
[3]
Radominski SC, Bernardo W, Paula AP, et al. Brazilian guidelines for the diagnosis and treatment of postmenopausal osteoporosis. Rev Bras Reumatol Engl Ed 2017; 57(Suppl. 2): 452-66.
[http://dx.doi.org/10.1016/j.rbr.2017.06.001] [PMID: 28838768]
[4]
Loures MAR, Zerbini CAF, Danowski JS, et al. Guidelines of the Brazilian Society of Rheumatology for the diagnosis and treatment of osteoporosis in men. Rev Bras Reumatol Engl Ed 2017; 57(Suppl. 2): 497-514.
[http://dx.doi.org/10.1016/j.rbr.2017.06.002] [PMID: 28800970]
[5]
Oliveira FC, Carvalho JO, Gusmão SBS, et al. High loads of nano-hydroxyapatite/graphene nanoribbon composites guided bone regeneration using an osteoporotic animal model. Int J Nanomedicine 2019; 14: 865-74.
[http://dx.doi.org/10.2147/IJN.S192456] [PMID: 30774339]
[6]
Khajuria DK, Razdan R, Mahapatra DR. Drugs for the management of osteoporosis: A review. Rev Bras Reumatol 2011; 51(4): 365-371, 379-382.
[PMID: 21779712]
[7]
Shirke SS, Jadhav SR, Jagtap AG. Methanolic extract of Cuminum cyminum inhibits ovariectomy-induced bone loss in rats. Exp Biol Med (Maywood) 2008; 233(11): 1403-10.
[http://dx.doi.org/10.3181/0803-RM-93] [PMID: 18824723]
[8]
Dawson-Hughes B, Harris SS, Krall EA, Dallal GE. Effect of calcium and vitamin D supplementation on bone density in men and women 65 years of age or older. N Engl J Med 1997; 337(10): 670-6.
[http://dx.doi.org/10.1056/NEJM199709043371003] [PMID: 9278463]
[9]
Zhao JG, Zeng XT, Wang J, Liu L. Association between calcium or vitamin D supplementation and fracture incidence in community-dwelling older adults: A systematic review and meta-analysis. JAMA 2017; 318(24): 2466-82.
[http://dx.doi.org/10.1001/jama.2017.19344] [PMID: 29279934]
[10]
Crisp AJ. Pizotifen to prevent side-effects of calcitonin. Lancet 1981; 1(8223): 775.
[http://dx.doi.org/10.1016/S0140-6736(81)92642-8] [PMID: 6110970]
[11]
Gennari C, Passeri M, Chierichetti SM, Piolini M. Side-effects of synthetic salmon and human calcitonin. Lancet 1983; 1(8324): 594-5.
[http://dx.doi.org/10.1016/S0140-6736(83)92846-5] [PMID: 6131289]
[12]
Karatoprak C, Kayatas K, Kilicaslan H, et al. Severe hypercalcemia due to teriparatide. Indian J Pharmacol 2012; 44(2): 270-1.
[http://dx.doi.org/10.4103/0253-7613.93869] [PMID: 22529492]
[13]
McMahon RE, Wang L, Skoracki R, Mathur AB. Development of nanomaterials for bone repair and regeneration. J Biomed Mater Res B Appl Biomater 2013; 101(2): 387-97.
[http://dx.doi.org/10.1002/jbm.b.32823] [PMID: 23281143]
[14]
Alencastre I, Sousa D, Alves C, et al. Delivery of pharmaceutics to bone: Nanotechnologies, high-throughput processing and in silico mathematical models. Eur Cell Mater 2016; 31: 355-81.
[http://dx.doi.org/10.22203/eCM.v031a23] [PMID: 27232664]
[15]
Zanin H, Saito E, Marciano FR, et al. Fast preparation of nano-hydroxyapatite/superhydrophilic reduced graphene oxide composites for bioactive applications. J Mater Chem B Mater Biol Med 2013; 1(38): 4947-55.
[http://dx.doi.org/10.1039/c3tb20550a] [PMID: 32261084]
[16]
Lobo AO, Corat MAF, Ramos SC, et al. Fast preparation of hydroxyapatite/superhydrophilic vertically aligned multiwalled carbon nanotube composites for bioactive application. Langmuir 2010; 26(23): 18308-14.
[http://dx.doi.org/10.1021/la1034646] [PMID: 20961085]
[17]
Ren X, Sun Z, Ma X, et al. Alginate-mediated mineralization for ultrafine hydroxyapatite hybrid nanoparticles. Langmuir 2018; 34(23): 6797-805.
[http://dx.doi.org/10.1021/acs.langmuir.8b00151] [PMID: 29771537]
[18]
Ren X, Yi Z, Sun Z, et al. Natural polysaccharide-incorporated hydroxyapatite as size-changeable, nuclear-targeted nanocarrier for efficient cancer therapy. Biomater Sci 2020; 8(19): 5390-401.
[http://dx.doi.org/10.1039/D0BM01320J] [PMID: 32996951]
[19]
Zhang K, Zhou Y, Xiao C, et al. Application of hydroxyapatite nanoparticles in tumor-associated bone segmental defect. Sci Adv 2019; 5(8): eaax6946.
[http://dx.doi.org/10.1126/sciadv.aax6946] [PMID: 31414050]
[20]
Ahmad M, Ahmed S, Swami BL, Ikram S. Preparation and characterization of antibacterial thiosemicarbazide chitosan as efficient Cu(II) adsorbent. Carbohydr Polym 2015; 132: 164-72.
[http://dx.doi.org/10.1016/j.carbpol.2015.06.034] [PMID: 26256337]
[21]
Croisier F, Jérôme C. Chitosan-based biomaterials for tissue engineering. Eur Polym J 2013; 49(4): 780-92.
[http://dx.doi.org/10.1016/j.eurpolymj.2012.12.009]
[22]
Kravanja G, Primožič M, Knez Ž, Leitgeb M. Chitosan-based (nano)materials for novel biomedical applications. Molecules 2019; 24(10): 1960.
[http://dx.doi.org/10.3390/molecules24101960] [PMID: 31117310]
[23]
Chatzipetros E, Christopoulos P, Donta C, et al. Application of nano-hydroxyapatite/chitosan scaffolds on rat calvarial critical-sized defects: A pilot study. Med Oral Patol Oral Cir Bucal 2018; 23(5): e625-32.
[http://dx.doi.org/10.4317/medoral.22455] [PMID: 30148464]
[24]
Russell AD, Hugo WB. Antimicrobial activity and action of silver. In Progress in Medicinal Chemistry 1994; 31: 351-70.
[http://dx.doi.org/10.1016/S0079-6468(08)70024-9]
[25]
Zhang R, Lee P, Lui VCH, et al. Silver nanoparticles promote osteogenesis of mesenchymal stem cells and improve bone fracture healing in osteogenesis mechanism mouse model. Nanomedicine 2015; 11(8): 1949-59.
[http://dx.doi.org/10.1016/j.nano.2015.07.016] [PMID: 26282383]
[26]
Martínez-Sanmiguel JJG, Zarate-Triviño D, Hernandez-Delgadillo R, et al. Anti-inflammatory and antimicrobial activity of bioactive hydroxyapatite/silver nanocomposites. J Biomater Appl 2019; 33(10): 1314-26.
[http://dx.doi.org/10.1177/0885328219835995] [PMID: 30880564]
[27]
Łapaj Ł, Woźniak W, Markuszewski J. Osseointegration of hydroxyapatite coatings doped with silver nanoparticles: Scanning electron microscopy studies on a rabbit model. Folia Morphol (Warsz) 2019; 78(1): 107-13.
[PMID: 30009369]
[28]
Yubao L, Klein CPAT, de Wijn J, et al. Morphology and phase structure of nanograde boneapatite-like rodshaped crystals Bioceramics. Philadelphia, USA: Butterworth-Heinemann 1993; pp. 173-8.
[29]
Yubao L, De Groot K, De Wijn J, Klein CPAT, Meer SVD. Morphology and composition of nanograde calcium phosphate needle-like crystals formed by simple hydrothermal treatment. J Mater Sci Mater Med 1994; 5(6–7): 326-31.
[http://dx.doi.org/10.1007/BF00058956]
[30]
Jarcho M, Kay JF, Gumaer KI, Doremus RH, Drobeck HP. Tissue, cellular and subcellular events at a bone-ceramic hydroxylapatite interface. J Bioeng 1977; 1(2): 79-92.
[PMID: 355244]
[31]
Paz A, Guadarrama D, López M, et al. A comparative study of hydroxyapatite nanoparticles synthesized by different routes. Quim Nova 2012; 35(9): 1724-7.
[http://dx.doi.org/10.1590/S0100-40422012000900004]
[32]
Calvo P, Remun͂ ́an-Ĺopez C, Vila-Jato JL, et al. Novel hydrophilic chitosan-polyethylene oxide nanoparticles as protein carriers. J Appl Polym Sci 1997; 63(1): 125-32.
[http://dx.doi.org/10.1002/(SICI)1097-4628(19970103)63:1<125::AID-APP13>3.0.CO;2-4]
[33]
Fernández-Urrusuno R, Calvo P, Remuñán-López C, Vila-Jato JL, Alonso MJ. Enhancement of nasal absorption of insulin using chitosan nanoparticles. Pharm Res 1999; 16(10): 1576-81.
[http://dx.doi.org/10.1023/A:1018908705446] [PMID: 10554100]
[34]
Grenha A, Seijo B, Remuñán-López C. Microencapsulated chitosan nanoparticles for lung protein delivery. Eur J Pharm Sci 2005; 25(4-5): 427-37.
[http://dx.doi.org/10.1016/j.ejps.2005.04.009] [PMID: 15893461]
[35]
Nikpour MR, Rabiee SM, Jahanshahi M. Synthesis and characterization of hydroxyapatite/chitosan nanocomposite materials for medical engineering applications. Compos, Part B Eng 2012; 43(4): 1881-6.
[http://dx.doi.org/10.1016/j.compositesb.2012.01.056]
[36]
Ciobanu CS, Iconaru SL, Le Coustumer P, Constantin LV, Predoi D. Antibacterial activity of silver-doped hydroxyapatite nanoparticles against gram-positive and gram-negative bacteria. Nanoscale Res Lett 2012; 7(1): 324.
[http://dx.doi.org/10.1186/1556-276X-7-324] [PMID: 22721352]
[37]
Mattila P. Dietary xylitol in the prevention of experimental osteoporosis: Beneficial effects on bone resorption, structure and biomechanics 1999.
[38]
Power RA, Iwaniec UT, Magee KA, Mitova-Caneva NG, Wronski TJ. Basic fibroblast growth factor has rapid bone anabolic effects in ovariectomized rats. Osteoporos Int 2004; 15(9): 716-23.
[http://dx.doi.org/10.1007/s00198-004-1595-4] [PMID: 15052380]
[39]
Aoki H, Aoki H, Kutsuno T, Li W, Niwa M. An in vivo study on the reaction of hydroxyapatite-sol injected into blood. J Mater Sci Mater Med 2000; 11(2): 67-72.
[http://dx.doi.org/10.1023/A:1008993814033] [PMID: 15348049]
[40]
Zhang C, Qu G, Sun Y, et al. Pharmacokinetics, biodistribution, efficacy and safety of N-octyl-O-sulfate chitosan micelles loaded with paclitaxel. Biomaterials 2008; 29(9): 1233-41.
[http://dx.doi.org/10.1016/j.biomaterials.2007.11.029] [PMID: 18093646]
[41]
Hadrup N, Loeschner K, Mortensen A, et al. The similar neurotoxic effects of nanoparticulate and ionic silver in vivo and in vitro. Neurotoxicology 2012; 33(3): 416-23.
[http://dx.doi.org/10.1016/j.neuro.2012.04.008] [PMID: 22531227]
[42]
Chen GX, Zheng S, Qin S, et al. Effect of low-magnitude whole-body vibration combined with alendronate in ovariectomized rats: A random controlled osteoporosis prevention study. PLoS One 2014; 9(5): e96181.
[http://dx.doi.org/10.1371/journal.pone.0096181] [PMID: 24796785]
[43]
Chin KY, Abdul-Majeed S, Mohamed N, Ima-Nirwana S. The effects of tocotrienol and lovastatin co-supplementation on bone dynamic histomorphometry and bone morphogenetic protein-2 expression in rats with estrogen deficiency. Nutrients 2017; 9(2): 143.
[http://dx.doi.org/10.3390/nu9020143] [PMID: 28212283]
[44]
Zhu H, Wang Z, Wang W. Effects of drynariae rhizoma total flavonoids on Smad1 and Smad5 mRNA Expression in Osteoporotic Rats. Life Sci J 2013; 10(3): 1213-7.
[45]
Banchroft J, Steven A, Turner D. Theory and practice of histopathological techniques. 4th ed. USA: Churchil Livingstone 1996.
[46]
Zhang XF, Liu ZG, Shen W, Gurunathan S. Silver nanoparticles: Synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci 2016; 17(9): 1501-34.
[http://dx.doi.org/10.3390/ijms17091534] [PMID: 27649147]
[47]
Fissan H, Ristig S, Kaminski H, Asbach C, Epple M. Comparison of different characterization methods for nanoparticle dispersions before and after aerosolization. Anal Methods 2014; 6(18): 7324-34.
[http://dx.doi.org/10.1039/C4AY01203H]
[48]
Berne BJ, Pecora R. Dynamic light scattering: With applications to chemistry, biology, and physics. USA: Courier Corporation 2000.
[49]
Koppel DE. Analysis of macromolecular polydispersity in intensity correlation spectroscopy: The method of cumulants. J Chem Phys 1972; 57(11): 4814-20.
[http://dx.doi.org/10.1063/1.1678153]
[50]
Dieckmann Y, Cölfen H, Hofmann H, Petri-Fink A. Particle size distribution measurements of manganese-doped ZnS nanoparticles. Anal Chem 2009; 81(10): 3889-95.
[http://dx.doi.org/10.1021/ac900043y] [PMID: 19374425]
[51]
Bhattacharjee S. DLS and zeta potential - What they are and what they are not? J Control Release 2016; 235: 337-51.
[http://dx.doi.org/10.1016/j.jconrel.2016.06.017] [PMID: 27297779]
[52]
Piccirillo C, Fernández-Arias M, Boutinguiza M, et al. Increased UV absorption properties of natural hydroxyapatite-based sunscreen through laser ablation modification in liquid. J Am Ceram Soc 2019; 102(6): 3163-74.
[http://dx.doi.org/10.1111/jace.16209]
[53]
Salimi MN, Bridson RH, Grover LM, Leeke GA. Effect of processing conditions on the formation of hydroxyapatite nanoparticles. Powder Technol 2012; 218: 109-18.
[http://dx.doi.org/10.1016/j.powtec.2011.11.049]
[54]
Predoi D, Iconaru SL, Buton N, Badea ML, Marutescu L. Antimicrobial activity of new materials based on lavender and basil essential oils and hydroxyapatite. Nanomaterials (Basel) 2018; 8(5): 291.
[http://dx.doi.org/10.3390/nano8050291] [PMID: 29710862]
[55]
Teow Y, Asharani PV, Hande MP, Valiyaveettil S. Health impact and safety of engineered nanomaterials. Chem Commun (Camb) 2011; 47(25): 7025-38.
[http://dx.doi.org/10.1039/c0cc05271j] [PMID: 21479319]
[56]
Patil S, Sandberg A, Heckert E, Self W, Seal S. Protein adsorption and cellular uptake of cerium oxide nanoparticles as a function of zeta potential. Biomaterials 2007; 28(31): 4600-7.
[http://dx.doi.org/10.1016/j.biomaterials.2007.07.029] [PMID: 17675227]
[57]
Núñez D, Elgueta E, Varaprasad K, Oyarzún P. Hydroxyapatite nanocrystals synthesized from calcium rich bio-wastes. Mater Lett 2018; 230: 64-8.
[http://dx.doi.org/10.1016/j.matlet.2018.07.077]
[58]
Ha S-W, Jang HL, Nam KT, Beck GR Jr. Nano-hydroxyapatite modulates osteoblast lineage commitment by stimulation of DNA methylation and regulation of gene expression. Biomaterials 2015; 65: 32-42.
[http://dx.doi.org/10.1016/j.biomaterials.2015.06.039] [PMID: 26141836]
[59]
Knowles JC, Callcut S, Georgiou G. Characterisation of the rheological properties and zeta potential of a range of hydroxyapatite powders. Biomaterials 2000; 21(13): 1387-92.
[http://dx.doi.org/10.1016/S0142-9612(00)00032-6] [PMID: 10850933]
[60]
Yamaguchi I, Iizuka S, Osaka A, Monma H, Tanaka J. The effect of citric acid addition on chitosan/hydroxyapatite composites. Colloids Surf A Physicochem Eng Asp 2003; 214(1–3): 111-8.
[http://dx.doi.org/10.1016/S0927-7757(02)00365-5]
[61]
Clogston JD, Patri AK. Zeta potential measurement Characterization of nanoparticles intended for drug delivery. Humana Press: USA 2011; pp. 63-70.
[http://dx.doi.org/10.1007/978-1-60327-198-1_6]
[62]
Shi C, Gao J, Wang M, Fu J, Wang D, Zhu Y. Ultra-trace silver-doped hydroxyapatite with non-cytotoxicity and effective antibacterial activity. Mater Sci Eng C 2015; 55: 497-505.
[http://dx.doi.org/10.1016/j.msec.2015.05.078] [PMID: 26117782]
[63]
Chen L, Mccrate JM, Lee JC, Li H. The role of surface charge on the uptake and biocompatibility of hydroxyapatite nanoparticles with osteoblast cells. Nanotechnology 2011; 22(10): 105708.
[http://dx.doi.org/10.1088/0957-4484/22/10/105708] [PMID: 21289408]
[64]
Doat A, Pellé F, Gardant N, Lebugle A. Synthesis of luminescent bioapatite nanoparticles for utilization as a biological probe. J Solid State Chem 2004; 177(4-5): 1179-87.
[http://dx.doi.org/10.1016/j.jssc.2003.10.023]
[65]
Swain SK, Dorozhkin SV, Sarkar D. Synthesis and dispersion of hydroxyapatite nanopowders. Mater Sci Eng C 2012; 32(5): 1237-40.
[http://dx.doi.org/10.1016/j.msec.2012.03.014]
[66]
Rameshbabu N, Sampath Kumar TS, Prabhakar TG, Sastry VS, Murty KVGK, Prasad Rao K. Antibacterial nanosized silver substituted hydroxyapatite: Synthesis and characterization. J Biomed Mater Res A 2007; 80(3): 581-91.
[http://dx.doi.org/10.1002/jbm.a.30958] [PMID: 17031822]
[67]
Ehrlich H, Krajewska B, Hanke T, et al. Chitosan membrane as a template for hydroxyapatite crystal growth in a model dual membrane diffusion system. J Membr Sci 2006; 237(1-2): 124-8.
[http://dx.doi.org/10.1016/j.memsci.2005.11.050]
[68]
Rajiv Gandhi M, Kousalya GN, Meenakshi S. Removal of copper(II) using chitin/chitosan nano-hydroxyapatite composite. Int J Biol Macromol 2011; 48(1): 119-24.
[http://dx.doi.org/10.1016/j.ijbiomac.2010.10.009] [PMID: 20970443]
[69]
Mohammad AM, Salah Eldin TA, Hassan MA, El-Anadouli BE. Efficient treatment of lead-containing wastewater by hydroxyapatite/chitosan nanostructures. Arab J Chem 2017; 10(5): 683-90.
[http://dx.doi.org/10.1016/j.arabjc.2014.12.016]
[70]
Bourtoom T, Chinnan MS. Preparation and properties of rice starch–chitosan blend biodegradable film. Lebensm Wiss Technol 2008; 41(9): 1633-41.
[http://dx.doi.org/10.1016/j.lwt.2007.10.014]
[71]
Yamaguchi I, Itoh S, Suzuki M, Osaka A, Tanaka J. The chitosan prepared from crab tendons: II. The chitosan/apatite composites and their application to nerve regeneration. Biomaterials 2003; 24(19): 3285-92.
[http://dx.doi.org/10.1016/S0142-9612(03)00163-7] [PMID: 12763456]
[72]
Ciobanu CS, Andronescu E, Vasile BS, et al. Looking for new synthesis of hydroxyapatite doped with europium. J Optoelectron Adv Mater 2010; 4(10): 1515-9.
[73]
Bai X, More K, Rouleau CM, Rabiei A. Functionally graded hydroxyapatite coatings doped with antibacterial components. Acta Biomater 2010; 6(6): 2264-73.
[http://dx.doi.org/10.1016/j.actbio.2009.12.002] [PMID: 19969112]
[74]
Ciobanu CS, Iconaru SL, Chifiriuc MC, Costescu A, Le Coustumer P, Predoi D. Synthesis and antimicrobial activity of silver-doped hydroxyapatite nanoparticles. BioMed Res Int 2013; 2013: 916218.
[http://dx.doi.org/10.1155/2013/916218] [PMID: 23509801]
[75]
Predoi D, Ghita RV, Costache M, et al. Characteristics of hydroxyapatite thin films. J Optoelectron Adv Mater 2007; 9(12): 3827-31.
[76]
Costescu A, Pasuk I, Ungureanu F, et al. Physico-chemical properties of nano-sized hexagonal hydroxyapatite powder synthesized by sol-gel. Dig J Nanomater Biostruct 2010; 5(4): 989-1000.
[77]
Alexis F, Pridgen E, Molnar LK, Farokhzad OC. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol Pharm 2008; 5(4): 505-15.
[http://dx.doi.org/10.1021/mp800051m] [PMID: 18672949]
[78]
Zheng J, Zhou W. In vivo imaging of nano-hydroxyapatite biodistribution using positron emission tomography imaging. Chem Lett 2012; 41(12): 1606-7.
[http://dx.doi.org/10.1246/cl.2012.1606]
[79]
Haidong L, Fang Y, Bo Y, et al. Effect of dietary soy isoflavones on bone loss in ovariectomized rats. Trop J Pharm Res 2018; 17(1): 91-6.
[http://dx.doi.org/10.4314/tjpr.v17i1.14]
[80]
Nakashima K, Zhou X, Kunkel G, et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 2002; 108(1): 17-29.
[http://dx.doi.org/10.1016/S0092-8674(01)00622-5] [PMID: 11792318]
[81]
Nishio Y, Dong Y, Paris M, O’Keefe RJ, Schwarz EM, Drissi H. Runx2-mediated regulation of the zinc finger Osterix/Sp7 gene. Gene 2006; 372: 62-70.
[http://dx.doi.org/10.1016/j.gene.2005.12.022] [PMID: 16574347]
[82]
Sun M, Zhou X, Chen L, et al. The regulatory roles of microRNAs in bone remodeling and perspectives as biomarkers in osteoporosis. BioMed Res Int 2016; 2016: 1652417.
[http://dx.doi.org/10.1155/2016/1652417] [PMID: 27073801]
[83]
Felber K, Elks PM, Lecca M, Roehl HH. Expression of osterix is Regulated by FGF and Wnt/β-Catenin signalling during osteoblast differentiation. PLoS One 2015; 10(12): e0144982.
[http://dx.doi.org/10.1371/journal.pone.0144982] [PMID: 26689368]
[84]
Kim B-J, Bae SJ, Lee S-Y, et al. TNF-α mediates the stimulation of sclerostin expression in an estrogen-deficient condition. Biochem Biophys Res Commun 2012; 424(1): 170-5.
[http://dx.doi.org/10.1016/j.bbrc.2012.06.100] [PMID: 22735261]
[85]
Li X, Zhang Y, Kang H, et al. Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J Biol Chem 2005; 280(20): 19883-7.
[http://dx.doi.org/10.1074/jbc.M413274200] [PMID: 15778503]
[86]
Gilbert L, He X, Farmer P, et al. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2α A) is inhibited by tumor necrosis factor-α. J Biol Chem 2002; 277(4): 2695-701.
[http://dx.doi.org/10.1074/jbc.M106339200] [PMID: 11723115]
[87]
Thorfve A, Lindahl C, Xia W, et al. Hydroxyapatite coating affects the Wnt signaling pathway during peri-implant healing in vivo. Acta Biomater 2014; 10(3): 1451-62.
[http://dx.doi.org/10.1016/j.actbio.2013.12.012] [PMID: 24342040]
[88]
Lü X, Wang J, Li B, Zhang Z, Zhao L. Gene expression profile study on osteoinductive effect of natural hydroxyapatite. J Biomed Mater Res A 2014; 102(8): 2833-41.
[http://dx.doi.org/10.1002/jbm.a.34951] [PMID: 24115491]
[89]
Song J-H, Kim J-H, Park S, et al. Signaling responses of osteoblast cells to hydroxyapatite: The activation of ERK and SOX9. J Bone Miner Metab 2008; 26(2): 138-42.
[http://dx.doi.org/10.1007/s00774-007-0804-6] [PMID: 18301969]
[90]
Guo J, Meng Z, Chen G, et al. Restoration of critical-size defects in the rabbit mandible using porous nanohydroxyapatite-polyamide scaffolds. Tissue Eng Part A 2012; 18(11-12): 1239-52.
[http://dx.doi.org/10.1089/ten.tea.2011.0503] [PMID: 22320360]
[91]
Cameron K, Travers P, Chander C, Buckland T, Campion C, Noble B. Directed osteogenic differentiation of human mesenchymal stem/precursor cells on silicate substituted calcium phosphate. J Biomed Mater Res A 2013; 101(1): 13-22.
[http://dx.doi.org/10.1002/jbm.a.34261] [PMID: 22733430]
[92]
He W, Andersson M, de Souza PPC, et al. Osteogenesis-inducing calcium phosphate nanoparticle precursors applied to titanium surfaces. Biomed Mater 2013; 8(3): 035007.
[http://dx.doi.org/10.1088/1748-6041/8/3/035007] [PMID: 23558249]
[93]
Lü L-X, Zhang X-F, Wang Y-Y, et al. Effects of hydroxyapatite-containing composite nanofibers on osteogenesis of mesenchymal stem cells in vitro and bone regeneration in vivo. ACS Appl Mater Interfaces 2013; 5(2): 319-30.
[http://dx.doi.org/10.1021/am302146w] [PMID: 23267692]
[94]
Peng H, Yin Z, Liu H, et al. Electrospun biomimetic scaffold of hydroxyapatite/chitosan supports enhanced osteogenic differentiation of mMSCs. Nanotechnology 2012; 23(48): 485102.
[http://dx.doi.org/10.1088/0957-4484/23/48/485102] [PMID: 23128604]
[95]
Pereira-Junior OCM, Rahal SC, Lima-Neto JF, Landim-Alvarenga Fda C, Monteiro FOB. In vitro evaluation of three different biomaterials as scaffolds for canine mesenchymal stem cells. Acta Cir Bras 2013; 28(5): 353-60.
[http://dx.doi.org/10.1590/S0102-86502013000500006] [PMID: 23702937]
[96]
Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. Osf2/Cbfa1: A transcriptional activator of osteoblast differentiation. Cell 1997; 89(5): 747-54.
[http://dx.doi.org/10.1016/S0092-8674(00)80257-3] [PMID: 9182762]
[97]
Miller J, Horner A, Stacy T, et al. The core-binding factor beta subunit is required for bone formation and hematopoietic maturation. Nat Genet 2002; 32(4): 645-9.
[http://dx.doi.org/10.1038/ng1049] [PMID: 12434155]
[98]
Lee M-H, Kwon T-G, Park H-S, Wozney JM, Ryoo H-M. BMP-2-induced Osterix expression is mediated by Dlx5 but is independent of Runx2. Biochem Biophys Res Commun 2003; 309(3): 689-94.
[http://dx.doi.org/10.1016/j.bbrc.2003.08.058] [PMID: 12963046]
[99]
Lee M-H, Kim Y-J, Kim H-J, et al. BMP-2-induced Runx2 expression is mediated by Dlx5, and TGF-beta 1 opposes the BMP-2-induced osteoblast differentiation by suppression of Dlx5 expression. J Biol Chem 2003; 278(36): 34387-94.
[http://dx.doi.org/10.1074/jbc.M211386200] [PMID: 12815054]
[100]
Wang L, Rao RR, Stegemann JP. Delivery of mesenchymal stem cells in chitosan/collagen microbeads for orthopedic tissue repair. Cells Tissues Organs 2013; 197(5): 333-43.
[http://dx.doi.org/10.1159/000348359] [PMID: 23571151]
[101]
Ma X-Y, Feng Y-F, Wang T-S, et al. Involvement of FAK-mediated BMP-2/Smad pathway in mediating osteoblast adhesion and differentiation on nano-HA/chitosan composite coated titanium implant under diabetic conditions. Biomater Sci 2017; 6(1): 225-38.
[http://dx.doi.org/10.1039/C7BM00652G] [PMID: 29231215]
[102]
Mathews S, Gupta PK, Bhonde R, Totey S. Chitosan enhances mineralization during osteoblast differentiation of human bone marrow-derived mesenchymal stem cells, by upregulating the associated genes. Cell Prolif 2011; 44(6): 537-49.
[http://dx.doi.org/10.1111/j.1365-2184.2011.00788.x] [PMID: 22011046]
[103]
Ho MH, Liao MH, Lin YL, Lai CH, Lin PI, Chen RM. Improving effects of chitosan nanofiber scaffolds on osteoblast proliferation and maturation. Int J Nanomedicine 2014; 9(1): 4293-304.
[PMID: 25246786]
[104]
Liu H, Peng H, Wu Y, et al. The promotion of bone regeneration by nanofibrous hydroxyapatite/chitosan scaffolds by effects on integrin-BMP/Smad signaling pathway in BMSCs. Biomaterials 2013; 34(18): 4404-17.
[http://dx.doi.org/10.1016/j.biomaterials.2013.02.048] [PMID: 23515177]
[105]
Mahmood M, Li Z, Casciano D, et al. Nanostructural materials increase mineralization in bone cells and affect gene expression through miRNA regulation. J Cell Mol Med 2011; 15(11): 2297-306.
[http://dx.doi.org/10.1111/j.1582-4934.2010.01234.x] [PMID: 21143388]
[106]
Qing T, Mahmood M, Zheng Y, Biris AS, Shi L, Casciano DA. A genomic characterization of the influence of silver nanoparticles on bone differentiation in MC3T3-E1 cells. J Appl Toxicol 2018; 38(2): 172-9.
[http://dx.doi.org/10.1002/jat.3528] [PMID: 28975650]
[107]
Lee K-S, Kim H-J, Li Q-L, et al. 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. Mol Cell Biol 2000; 20(23): 8783-92.
[http://dx.doi.org/10.1128/MCB.20.23.8783-8792.2000] [PMID: 11073979]
[108]
Li Z, Hassan MQ, Volinia S, et al. A microRNA signature for a BMP2-induced osteoblast lineage commitment program. Proc Natl Acad Sci USA 2008; 105(37): 13906-11.
[http://dx.doi.org/10.1073/pnas.0804438105] [PMID: 18784367]
[109]
Ali IHA, Brazil DP. Bone morphogenetic proteins and their antagonists: Current and emerging clinical uses. Br J Pharmacol 2014; 171(15): 3620-32.
[http://dx.doi.org/10.1111/bph.12724] [PMID: 24758361]
[110]
Liu H, Xu GW, Wang YF, et al. Composite scaffolds of nano-hydroxyapatite and silk fibroin enhance mesenchymal stem cell-based bone regeneration via the interleukin 1 alpha autocrine/paracrine signaling loop. Biomaterials 2015; 49: 103-12.
[http://dx.doi.org/10.1016/j.biomaterials.2015.01.017] [PMID: 25725559]
[111]
ten Dijke P, Miyazono K, Heldin C-H. Signaling inputs converge on nuclear effectors in TGF-β signaling. Trends Biochem Sci 2000; 25(2): 64-70.
[http://dx.doi.org/10.1016/S0968-0004(99)01519-4] [PMID: 10664585]
[112]
Shi Y, Massagué J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 2003; 113(6): 685-700.
[http://dx.doi.org/10.1016/S0092-8674(03)00432-X] [PMID: 12809600]
[113]
Chen D, Zhao M, Harris SE, Mi Z. Signal transduction and biological functions of bone morphogenetic proteins. Front Biosci 2004; 9(1-3): 349-58.
[http://dx.doi.org/10.2741/1090] [PMID: 14766372]
[114]
Chen G, Deng C, Li YP. TGF-β and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci 2012; 8(2): 272-88.
[http://dx.doi.org/10.7150/ijbs.2929] [PMID: 22298955]
[115]
Jian J, Sun L, Cheng X, Hu X, Liang J, Chen Y. Calycosin-7-O-β-d-glucopyranoside stimulates osteoblast differentiation through regulating the BMP/WNT signaling pathways. Acta Pharm Sin B 2015; 5(5): 454-60.
[http://dx.doi.org/10.1016/j.apsb.2015.06.005] [PMID: 26579475]
[116]
Yang X, Huo H, Xiu C, et al. Inhibition of osteoblast differentiation by aluminum trichloride exposure is associated with inhibition of BMP-2/Smad pathway component expression. Food Chem Toxicol 2016; 97: 120-6.
[http://dx.doi.org/10.1016/j.fct.2016.09.004] [PMID: 27600293]
[117]
Gong W, Zheng H, Li F, et al. Preventive and therapeutic effect of Corn Cervi Pantotrichum on bone tissue in ovariectomized rats through activation of BMP-2/Smads/Runx2 signal transduction pathway. Biomed Res (Aligarh) 2018; 29(12): 2602-8.
[118]
Zhou S, Turgeman G, Harris SE, et al. Estrogens activate bone morphogenetic protein-2 gene transcription in mouse mesenchymal stem cells. Mol Endocrinol 2003; 17(1): 56-66.
[http://dx.doi.org/10.1210/me.2002-0210] [PMID: 12511606]
[119]
Zhou S, Zilberman Y, Wassermann K, Bain SD, Sadovsky Y, Gazit D. Estrogen modulates estrogen receptor alpha and beta expression, osteogenic activity, and apoptosis in mesenchymal stem cells (MSCs) of osteoporotic mice. J Cell Biochem Suppl 2001; 81(S36)(Suppl. 36): 144-55.
[http://dx.doi.org/10.1002/jcb.1096] [PMID: 11455579]
[120]
Tang Z, Wang Z, Qing F, et al. Bone morphogenetic protein Smads signaling in mesenchymal stem cells affected by osteoinductive calcium phosphate ceramics. J Biomed Mater Res A 2015; 103(3): 1001-10.
[http://dx.doi.org/10.1002/jbm.a.35242] [PMID: 24889783]
[121]
Suto M, Nemoto E, Kanaya S, Suzuki R, Tsuchiya M, Shimauchi H. Nanohydroxyapatite increases BMP-2 expression via a p38 MAP kinase dependent pathway in periodontal ligament cells. Arch Oral Biol 2013; 58(8): 1021-8.
[http://dx.doi.org/10.1016/j.archoralbio.2013.02.014] [PMID: 23518236]
[122]
Tsai S-Y, Huang Y-L, Yang W-H, Tang C-H. Hepatocyte growth factor-induced BMP-2 expression is mediated by c-Met receptor, FAK, JNK, Runx2, and p300 pathways in human osteoblasts. Int Immunopharmacol 2012; 13(2): 156-62.
[http://dx.doi.org/10.1016/j.intimp.2012.03.026] [PMID: 22504529]
[123]
Qin H, Zhu C, An Z, et al. Silver nanoparticles promote osteogenic differentiation of human urine-derived stem cells at noncytotoxic concentrations. Int J Nanomedicine 2014; 9(1): 2469-78.
[http://dx.doi.org/10.2147/IJN.S59753] [PMID: 24899804]
[124]
Kang K, Lim DH, Choi IH, et al. Vascular tube formation and angiogenesis induced by polyvinylpyrrolidone-coated silver nanoparticles. Toxicol Lett 2011; 205(3): 227-34.
[http://dx.doi.org/10.1016/j.toxlet.2011.05.1033] [PMID: 21729742]
[125]
Mukherjee A, Rotwein P. Akt promotes BMP2-mediated osteoblast differentiation and bone development. J Cell Sci 2009; 122(Pt 5): 716-26.
[http://dx.doi.org/10.1242/jcs.042770] [PMID: 19208758]
[126]
Bai SY, Chen Y, Dai HW, Huang L. [Effect of sclerostin on the functions and related mechanisms of cementoblasts under mechanical stress West China. J Stomatol 2019; 37(2): 162-7.
[PMID: 31168982]
[127]
Wan M, Shi X, Feng X, Cao X. Transcriptional mechanisms of bone morphogenetic protein-induced osteoprotegrin gene expression. J Biol Chem 2001; 276(13): 10119-25.
[http://dx.doi.org/10.1074/jbc.M006918200] [PMID: 11139569]
[128]
Lu Z, Roohani-Esfahani S-I, Kwok PCL, Zreiqat H. Osteoblasts on rod shaped hydroxyapatite nanoparticles incorporated PCL film provide an optimal osteogenic niche for stem cell differentiation. Tissue Eng Part A 2011; 17(11-12): 1651-61.
[http://dx.doi.org/10.1089/ten.tea.2010.0567] [PMID: 21306280]
[129]
Biris AS, Casciano D, Mahmood M. Nanostructural materials that increase mineralization in bone cells and affect gene expression through miRNA regulation and applications of same. US Patent 2012/0244224A1, 2012.
[130]
Wang X, Zhang M, Zhang D, et al. Structural elucidation and anti-osteoporosis activities of polysaccharides obtained from Curculigo orchioides. Carbohydr Polym 2019; 203: 292-301.
[http://dx.doi.org/10.1016/j.carbpol.2018.09.059] [PMID: 30318216]
[131]
Turner RT, Maran A, Lotinun S, et al. Animal models for osteoporosis. Rev Endocr Metab Disord 2001; 2(1): 117-27.
[http://dx.doi.org/10.1023/A:1010067326811] [PMID: 11704974]
[132]
Zhou W, Liu Y, Shen J, et al. Melatonin increases bone mass around the prostheses of OVX rats by ameliorating mitochondrial oxidative stress via the SIRT3/SOD2 signaling pathway. Oxid Med Cell Longev 2019; 2019: Article ID 4019619. Available from:
[http://dx.doi.org/10.1155/2019/4019619]
[133]
Zhang J, Zong L, Bai D. Boeravinone B promotes fracture healing in ovariectomy-induced osteoporotic rats via the regulation of NF-κB p65/IκB -α/SIRT-1 signaling pathway. Trop J Pharm Res 2019; 18(5): 955-60.
[http://dx.doi.org/10.4314/tjpr.v18i5.7]
[134]
Yang HJ, Kim MJ, Qiu JY, et al. Rice porridge containing welsh onion root water extract alleviates osteoarthritis-related pain behaviors, glucose levels, and bone metabolism in osteoarthritis-induced ovariectomized rats. Nutrients 2019; 11(7): 1503.
[http://dx.doi.org/10.3390/nu11071503] [PMID: 31262076]
[135]
Mukherjee M, Das AS, Das D, Mukherjee S, Mitra S, Mitra C. Role of peritoneal macrophages and lymphocytes in the development of hypogonadal osteoporosis in an ovariectomized rat model: Possible phytoestrogenic efficacy of oil extract of garlic to preserve skeletal health. Phytother Res 2007; 21(11): 1045-54.
[http://dx.doi.org/10.1002/ptr.2209] [PMID: 17600860]
[136]
Zhao R, Xie P, Zhang K, et al. Selective effect of hydroxyapatite nanoparticles on osteoporotic and healthy bone formation correlates with intracellular calcium homeostasis regulation. Acta Biomater 2017; 59: 338-50.
[http://dx.doi.org/10.1016/j.actbio.2017.07.009] [PMID: 28698163]
[137]
Tao W, Kai Hui N, Jing Di C, et al. A new bone repair scaffold combined with chitosan/hydroxyapatite and sustained releasing icariin. Chin Sci Bull 2009; 54(17): 2953-61.
[http://dx.doi.org/10.1007/s11434-009-0250-z]
[138]
Chen S, Lau P, Lei M, et al. Segmental composite porous scaffolds with either osteogenesis or anti-bone resorption properties tested in a rabbit ulna defect model. J Tissue Eng Regen Med 2017; 11(1): 34-43.
[http://dx.doi.org/10.1002/term.1828] [PMID: 24668843]
[139]
Tsuang Y-H, Chen L-T, Chiang C-J, et al. Isoflavones prevent bone loss following ovariectomy in young adult rats. J Orthop Surg Res 2008; 3(1): 12.
[http://dx.doi.org/10.1186/1749-799X-3-12] [PMID: 18312690]
[140]
Jeong D-W, Kim E-Y, Kim J-H, et al. Lycopus lucidus Turcz inhibits the osteoclastogenesis in RAW 264.7 cells and bone loss in ovariectomized rat model. Evid-Based Complementary Altern Med 2019; 2019: Article ID 3231784. Available from:
[http://dx.doi.org/10.1155/2019/3231784]
[141]
Dave JR, Dewle AM, Mhaske ST, et al. Hydroxyapatite nanorods loaded with parathyroid hormone (PTH) synergistically enhance the net formative effect of PTH anabolic therapy. Nanomedicine 2019; 15(1): 218-30.
[http://dx.doi.org/10.1016/j.nano.2018.10.003] [PMID: 30343014]
[142]
Liu S, Zhou H, Liu H, Ji H, Fei W, Luo E. Fluorine-contained hydroxyapatite suppresses bone resorption through inhibiting osteoclasts differentiation and function in vitro and in vivo. Cell Prolif 2019; 52(3): e12613.
[http://dx.doi.org/10.1111/cpr.12613] [PMID: 30968984]
[143]
Abd El Moneim RA, Mahmoud SA. Histological study of the femur and the lumbar vertebrae in ovariectomized adult albino rats following administration of collagen hydrosylate. Egypt J Histol 2013; 36(3): 646-59.
[http://dx.doi.org/10.1097/01.EHX.0000434384.05294.02]
[144]
Cao H, Zhang W, Meng F, et al. Osteogenesis catalyzed by titanium-supported silver nanoparticles. ACS Appl Mater Interfaces 2017; 9(6): 5149-57.
[http://dx.doi.org/10.1021/acsami.6b15448] [PMID: 28111942]
[145]
Fossey S, Vahle J, Long P, et al. Nonproliferative and proliferative lesions of the rat and mouse skeletal tissues (bones, joints, and teeth). J Toxicol Pathol 2016; 29(Suppl. 3): 49S-103S.
[http://dx.doi.org/10.1293/tox.29.3S-2] [PMID: 27621538]
[146]
Ominsky MS, Niu Q-T, Li C, Li X, Ke HZ. Tissue-level mechanisms responsible for the increase in bone formation and bone volume by sclerostin antibody. J Bone Miner Res 2014; 29(6): 1424-30.
[http://dx.doi.org/10.1002/jbmr.2152] [PMID: 24967455]
[147]
Wang Y, Xue F. Effect of Bushen Jiangu decoction on ovariectomyinduced osteoporosis in rats. Trop J Pharm Res 2019; 18(2): 327.
[http://dx.doi.org/10.4314/tjpr.v18i2.15]
[148]
Liberman UA. Long-term safety of bisphosphonate therapy for osteoporosis: A review of the evidence. Drugs Aging 2006; 23(4): 289-98.
[http://dx.doi.org/10.2165/00002512-200623040-00002] [PMID: 16732688]
[149]
Reginster J-Y, Malaise O, Neuprez A, Jouret V-E, Close P. Intermittent bisphosphonate therapy in postmenopausal osteoporosis: Progress to date. Drugs Aging 2007; 24(5): 351-9.
[http://dx.doi.org/10.2165/00002512-200724050-00001] [PMID: 17503893]

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