Lactoferrin in Bone Tissue Regeneration

Author(s): Madalina Icriverzi, Valentina Dinca, Magdalena Moisei, Robert W. Evans, Mihaela Trif, Anca Roseanu*

Journal Name: Current Medicinal Chemistry

Volume 27 , Issue 6 , 2020

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Abstract:

Among the multiple properties exhibited by lactoferrin (Lf), its involvement in bone regeneration processes is of great interest at the present time. A series of in vitro and in vivo studies have revealed the ability of Lf to promote survival, proliferation and differentiation of osteoblast cells and to inhibit bone resorption mediated by osteoclasts. Although the mechanism underlying the action of Lf in bone cells is still not fully elucidated, it has been shown that its mode of action leading to the survival of osteoblasts is complemented by its mitogenic effect. Activation of several signalling pathways and gene expression, in an LRPdependent or independent manner, has been identified. Unlike the effects on osteoblasts, the action on osteoclasts is different, with Lf leading to a total arrest of osteoclastogenesis.

Due to the positive effect of Lf on osteoblasts, the potential use of Lf alone or in combination with different biologically active compounds in bone tissue regeneration and the treatment of bone diseases is of great interest. Since the bioavailability of Lf in vivo is poor, a nanotechnology- based strategy to improve the biological properties of Lf was developed. The investigated formulations include incorporation of Lf into collagen membranes, gelatin hydrogel, liposomes, loading onto nanofibers, porous microspheres, or coating onto silica/titan based implants. Lf has also been coupled with other biologically active compounds such as biomimetic hydroxyapatite, in order to improve the efficacy of biomaterials used in the regulation of bone homeostasis.

This review aims to provide an up-to-date review of research on the involvement of Lf in bone growth and healing and on its use as a potential therapeutic factor in bone tissue regeneration.

Keywords: Lactoferrin, osteoblast, osteoclast, bone, nanoformulations, regeneration.

[1]
Metz-Boutigue, M.H.; Jollès, J.; Mazurier, J.; Schoentgen, F.; Legrand, D.; Spik, G.; Montreuil, J.; Jollès, P. Human lactotransferrin: amino acid sequence and structural comparisons with other transferrins. Eur. J. Biochem., 1984, 145(3), 659-676.
[http://dx.doi.org/10.1111/j.1432-1033.1984.tb08607.x] [PMID: 6510420]
[2]
Lönnerdal, B.; Iyer, S. Lactoferrin: molecular structure and biological function. Annu. Rev. Nutr., 1995, 15, 93-110.
[http://dx.doi.org/10.1146/annurev.nu.15.070195.000521] [PMID: 8527233]
[3]
Masson, P.L.; Heremans, J.F.; Dive, C.H. An iron-binding protein common to many external secretions. Clin. Chim. Acta, 1966, 14, 735-739.
[http://dx.doi.org/10.1016/0009-8981(66)90004-0]
[4]
Masson, P.L.; Heremans, J.F.; Schonne, E. Lactoferrin, an iron-binding protein in neutrophilic leukocytes. J. Exp. Med., 1969, 130(3), 643-658.
[http://dx.doi.org/10.1084/jem.130.3.643] [PMID: 4979954 ]
[5]
Baggiolini, M.; De Duve, C.; Masson, P.L.; Heremans, J.F. Association of lactoferrin with specific granules in rabbit heterophil leukocytes. J. Exp. Med., 1970, 131(3), 559-570.
[http://dx.doi.org/10.1084/jem.131.3.559] [PMID: 5413328 ]
[6]
Caccavo, D.; Sebastiani, G.D.; Di Monaco, C.; Guido, F.; Galeazzi, M.; Ferri, G.M.; Bonomo, L.; Afeltra, A. Increased levels of lactoferrin in synovial fluid but not in serum from patients with rheumatoid arthritis. Int. J. Clin. Lab. Res., 1999, 29(1), 30-35.
[http://dx.doi.org/10.1007/s005990050059] [PMID: 10356661 ]
[7]
Haridas, M.; Anderson, B.F.; Baker, E.N. Structure of human diferric lactoferrin refined at 2.2 A resolution. Acta Crystallogr. D Biol. Crystallogr., 1995, 51(Pt 5), 629-646.
[http://dx.doi.org/10.1107/S0907444994013521] [PMID: 15299793 ]
[8]
Baker, E.N.; Baker, H.M. Molecular structure, binding properties and dynamics of lactoferrin. Cell. Mol. Life Sci., 2005, 62(22), 2531-2539.
[http://dx.doi.org/10.1007/s00018-005-5368-9] [PMID: 16261257 ]
[9]
Derisbourg, P.; Wieruszeski, J.M.; Montreuil, J.; Spik, G. Primary structure of glycans isolated from human leucocyte lactotransferrin. Absence of fucose residues questions the proposed mechanism of hyposideraemia. Biochem. J., 1990, 269(3), 821-825.
[http://dx.doi.org/10.1042/bj2690821] [PMID: 2390069 ]
[10]
Baker, H.M.; Baker, E.N. A structural perspective on lactoferrin function. Biochem. Cell Biol., 2012, 90(3), 320-328.
[http://dx.doi.org/10.1139/o11-071] [PMID: 22292559 ]
[11]
van Berkel, P.H.; Geerts, M.E.; van Veen, H.A.; Kooiman, P.M.; Pieper, F.R.; de Boer, H.A.; Nuijens, J.H. Glycosylated and unglycosylated human lactoferrins both bind iron and show identical affinities towards human lysozyme and bacterial lipopolysaccharide, but differ in their susceptibilities towards tryptic proteolysis. Biochem. J., 1995, 312(Pt 1), 107-114.
[http://dx.doi.org/10.1042/bj3120107] [PMID: 7492299 ]
[12]
Elass-Rochard, E.; Roseanu, A.; Legrand, D.; Trif, M.; Salmon, V.; Motas, C.; Montreuil, J.; Spik, G. Lactoferrin-lipopolysaccharide interaction: involvement of the 28-34 loop region of human lactoferrin in the high-affinity binding to Escherichia coli 055B5 lipopolysaccharide. Biochem. J., 1995, 312(Pt 3), 839-845.
[http://dx.doi.org/10.1042/bj3120839] [PMID: 8554529 ]
[13]
Elass-Rochard, E.; Legrand, D.; Salmon, V.; Roseanu, A.; Trif, M.; Tobias, P.S.; Mazurier, J.; Spik, G. Lactoferrin inhibits the endotoxin interaction with CD14 by competition with the lipopolysaccharide-binding protein. Infect. Immun., 1998, 66(2), 486-491.
[http://dx.doi.org/10.1128/IAI.66.2.486-491.1998] [PMID: 9453600 ]
[14]
Damiens, E.; El Yazidi, I.; Mazurier, J.; Elass-Rochard, E.; Duthille, I.; Spik, G.; Boilly-Marer, Y. Role of heparan sulphate proteoglycans in the regulation of human lactoferrin binding and activity in the MDA-MB-231 breast cancer cell line. Eur. J. Cell Biol., 1998, 77(4), 344-351.
[http://dx.doi.org/10.1016/S0171-9335(98)80093-9] [PMID: 9930659 ]
[15]
Farnaud, S.; Evans, R.W. Lactoferrin--a multifunctional protein with antimicrobial properties. Mol. Immunol., 2003, 40(7), 395-405.
[http://dx.doi.org/10.1016/S0161-5890(03)00152-4] [PMID: 14568385 ]
[16]
Legrand, D.; Elass, E.; Carpentier, M.; Mazurier, J. Lactoferrin: a modulator of immune and inflammatory responses. Cell. Mol. Life Sci., 2005, 62(22), 2549-2559.
[http://dx.doi.org/10.1007/s00018-005-5370-2] [PMID: 16261255 ]
[17]
Valenti, P.; Antonini, G. Lactoferrin: an important host defence against microbial and viral attack. Cell. Mol. Life Sci., 2005, 62(22), 2576-2587.
[http://dx.doi.org/10.1007/s00018-005-5372-0] [PMID: 16261253 ]
[18]
Roseanu, A.; Brock, J.H. What are the structure and the biological function of lactoferrin in human breast milk? IUBMB Life, 2006, 58(4), 235-237.
[http://dx.doi.org/10.1080/15216540600577897] [PMID: 16754302 ]
[19]
Actor, J.K.; Hwang, S.A.; Kruzel, M.L. Lactoferrin as a natural immune modulator. Curr. Pharm. Des., 2009, 15(17), 1956-1973.
[http://dx.doi.org/10.2174/138161209788453202] [PMID: 19519436 ]
[20]
van der Strate, B.W.; Beljaars, L.; Molema, G.; Harmsen, M.C.; Meijer, D.K. Antiviral activities of lactoferrin. Antiviral Res., 2001, 52(3), 225-239.
[http://dx.doi.org/10.1016/S0166-3542(01)00195-4] [PMID: 11675140 ]
[21]
Vogel, H.J. Lactoferrin, a bird’s eye view. Biochem. Cell Biol., 2012, 90(3), 233-244.
[http://dx.doi.org/10.1139/o2012-016] [PMID: 22540735 ]
[22]
Florian, P.E.; Lazar, C.; Nichita, N.; Roseanu, A. Antiviral activity of lactoferrin: from basic research to medical applications in: Viral Infections: Causes, Treatment Options and Potential Complications; Shinn, D., Ed.; Nova Science Publishers: NY, USA, 2014, pp. 205-246.
[23]
Legrand, D. Overview of lactoferrin as a natural immune modulator. J. Pediatr., 2016, 173(Suppl.), S10-S15.
[http://dx.doi.org/10.1016/j.jpeds.2016.02.071] [PMID: 27234406 ]
[24]
Cornish, J. Lactoferrin promotes bone growth. Biometals, 2004, 17(3), 331-335.
[http://dx.doi.org/10.1023/B:BIOM.0000027713.18694.91] [PMID: 15222486 ]
[25]
Humphrey, W.; Dalke, A.; Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph., 1996, 14(1), 33-38. 27- 28.
[http://dx.doi.org/10.1016/0263-7855(96)00018-5] [PMID: 8744570 ]
[26]
Cornish, J.; Callon, K.E.; Naot, D.; Palmano, K.P.; Banovic, T.; Bava, U.; Watson, M.; Lin, J.M.; Tong, P.C.; Chen, Q.; Chan, V.A.; Reid, H.E.; Fazzalari, N.; Baker, H.M.; Baker, E.N.; Haggarty, N.W.; Grey, A.B.; Reid, I.R. Lactoferrin is a potent regulator of bone cell activity and increases bone formation in vivo. Endocrinology, 2004, 145(9), 4366-4374.
[http://dx.doi.org/10.1210/en.2003-1307] [PMID: 15166119 ]
[27]
Park, S.Y.; Jeong, A.J.; Kim, G.Y.; Jo, A.; Lee, J.E.; Leem, S.H.; Yoon, J.H.; Ye, S.K.; Chung, J.W. Lactoferrin protects human mesenchymal stem cells from oxidative stress-induced senescence and apoptosis. J. Microbiol. Biotechnol., 2017, 27(10), 1877-1884.
[http://dx.doi.org/10.4014/jmb.1707.07040] [PMID: 28870012 ]
[28]
Grey, A.; Banovic, T.; Zhu, Q.; Watson, M.; Callon, K.; Palmano, K.; Ross, J.; Naot, D.; Reid, I.R.; Cornish, J. The low-density lipoprotein receptor-related protein 1 is a mitogenic receptor for lactoferrin in osteoblastic cells. Mol. Endocrinol., 2004, 18(9), 2268-2278.
[http://dx.doi.org/10.1210/me.2003-0456] [PMID: 15178744 ]
[29]
Naot, D.; Grey, A.; Reid, I.R.; Cornish, J. Lactoferrin--a novel bone growth factor. Clin. Med. Res., 2005, 3(2), 93-101.
[http://dx.doi.org/10.3121/cmr.3.2.93] [PMID: 16012127 ]
[30]
Grey, A.; Zhu, Q.; Watson, M.; Callon, K.; Cornish, J. Lactoferrin potently inhibits osteoblast apoptosis, via an LRP1-independent pathway. Mol. Cell. Endocrinol., 2006, 251(1-2), 96-102.
[http://dx.doi.org/10.1016/j.mce.2006.03.002] [PMID: 16650524 ]
[31]
Cornish, J.; Naot, D. Lactoferrin as an effector molecule in the skeleton. Biometals, 2010, 23(3), 425-430.
[http://dx.doi.org/10.1007/s10534-010-9320-6] [PMID: 20232111 ]
[32]
Naot, D.; Chhana, A.; Matthews, B.G.; Callon, K.E.; Tong, P.C.; Lin, J.M.; Costa, J.L.; Watson, M.; Grey, A.B.; Cornish, J. Molecular mechanisms involved in the mitogenic effect of lactoferrin in osteoblasts. Bone, 2011, 49(2), 217-224.
[http://dx.doi.org/10.1016/j.bone.2011.04.002] [PMID: 21515435 ]
[33]
Winslow, M.M.; Pan, M.; Starbuck, M.; Gallo, E.M.; Deng, L.; Karsenty, G.; Crabtree, G.R. Calcineurin/NFAT signaling in osteoblasts regulates bone mass. Dev. Cell, 2006, 10(6), 771-782.
[http://dx.doi.org/10.1016/j.devcel.2006.04.006] [PMID: 16740479 ]
[34]
Nakajima, K.; Kanno, Y.; Nakamura, M.; Gao, X.D.; Kawamura, A.; Itoh, F.; Ishisaki, A. Bovine milk lactoferrin induces synthesis of the angiogenic factors VEGF and FGF2 in osteoblasts via the p44/p42 MAP kinase pathway. Biometals, 2011, 24(5), 847-856.
[http://dx.doi.org/10.1007/s10534-011-9439-0] [PMID: 21404021 ]
[35]
Hou, J.M.; Chen, E.Y.; Lin, F.; Lin, Q.M.; Xue, Y.; Lan, X.H.; Wu, M. Lactoferrin induces osteoblast growth through IGF-1R. Int. J. Endocrinol., 2015, 2015282806
[http://dx.doi.org/10.1155/2015/282806] [PMID: 26290662 ]
[36]
Takayama, Y.; Mizumachi, K. Effect of bovine lactoferrin on extracellular matrix calcification by human osteoblast-like cells. Biosci. Biotechnol. Biochem., 2008, 72(1), 226-230.
[http://dx.doi.org/10.1271/bbb.70465] [PMID: 18175916]
[37]
Naot, D.; Palmano, K.; Cornish, J. Lactoferrin - a potential anabolic intervention in osteoporosis in: Osteoporosis; Dionyssiotis, Y., Ed.; InTech, 2012, pp. 803-820.
[38]
Matthews, B.G.; Naot, D.; Callon, K.E.; Musson, D.S.; Locklin, R.; Hulley, P.A.; Grey, A.; Cornish, J. Enhanced osteoblastogenesis in three-dimensional collagen gels. Bonekey Rep., 2014, 3, 560.
[http://dx.doi.org/10.1038/bonekey.2014.55] [PMID: 25120910 ]
[39]
Ying, X.; Cheng, S.; Wang, W.; Lin, Z.; Chen, Q.; Zhang, W.; Kou, D.; Shen, Y.; Cheng, X.; Peng, L.; Zi , Xu. H.; Zhu Lu, C. Effect of lactoferrin on osteogenic differentiation of human adipose stem cells. Int. Orthop., 2012, 36(3), 647-653.
[http://dx.doi.org/10.1007/s00264-011-1303-x] [PMID: 21713451 ]
[40]
Yagi, M.; Suzuki, N.; Takayama, T.; Arisue, M.; Kodama, T.; Yoda, Y.; Otsuka, K.; Ito, K. Effects of lactoferrin on the differentiation of pluripotent mesenchymal cells. Cell Biol. Int., 2009, 33(3), 283-289.
[http://dx.doi.org/10.1016/j.cellbi.2008.11.013] [PMID: 19103298 ]
[41]
Zhang, W.; Guo, H.; Jing, H.; Li, Y.; Wang, X.; Zhang, H.; Jiang, L.; Ren, F. Lactoferrin stimulates osteoblast differentiation through PKA and p38 pathways independent of lactoferrin’s receptor LRP1. J. Bone Miner. Res., 2014, 29(5), 1232-1243.
[http://dx.doi.org/10.1002/jbmr.2116] [PMID: 24877241 ]
[42]
Rey, A.; Manen, D.; Rizzoli, R.; Ferrari, S.L.; Caverzasio, J. Evidences for a role of p38 MAP kinase in the stimulation of alkaline phosphatase and matrix mineralization induced by parathyroid hormone in osteoblastic cells. Bone, 2007, 41(1), 59-67.
[http://dx.doi.org/10.1016/j.bone.2007.02.031] [PMID: 17434817 ]
[43]
Amini, A.A.; Nair, L.S. Recombinant human lactoferrin as a biomaterial for bone tissue engineering: mechanism of antiapoptotic and osteogenic activity. Adv. Healthc. Mater., 2014, 3(6), 897-905.
[http://dx.doi.org/10.1002/adhm.201300496] [PMID: 24352833]
[44]
Liu, M.; Fan, F.; Shi, P.; Tu, M.; Yu, C.; Yu, C.; Du, M. Lactoferrin promotes MC3T3-E1 osteoblast cells proliferation via MAPK signaling pathways Int J Biol Macromol, 2018, 107(Pt A), 137-143.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.08.151]
[45]
Zhang, J.L.; Han, X.; Shan, Y.J.; Zhang, L.W.; Du, M.; Liu, M.; Yi, H.X.; Ma, Y. Effect of bovine lactoferrin and human lactoferrin on the proliferative activity of the osteoblast cell line MC3T3-E1 in vitro. J. Dairy Sci., 2018, 101(3), 1827-1833.
[http://dx.doi.org/10.3168/jds.2017-13161] [PMID: 29290425 ]
[46]
Lorget, F.; Clough, J.; Oliveira, M.; Daury, M.C.; Sabokbar, A.; Offord, E. Lactoferrin reduces in vitro osteoclast differentiation and resorbing activity. Biochem. Biophys. Res. Commun., 2002, 296(2), 261-266.
[http://dx.doi.org/10.1016/S0006-291X(02)00849-5] [PMID: 12163011 ]
[47]
Yamano, E.; Miyauchi, M.; Furusyo, H.; Kawazoe, A.; Ishikado, A.; Makino, T.; Tanne, K.; Tanaka, E.; Takata, T. Inhibitory effects of orally administrated liposomal bovine lactoferrin on the LPS-induced osteoclastogenesis. Lab. Invest., 2010, 90(8), 1236-1246.
[http://dx.doi.org/10.1038/labinvest.2010.80] [PMID: 20421871 ]
[48]
Inubushi, T.; Kawazoe, A.; Miyauchi, M.; Kudo, Y.; Ao, M.; Ishikado, A.; Makino, T.; Takata, T. Molecular mechanisms of the inhibitory effects of bovine lactoferrin on lipopolysaccharide-mediated osteoclastogenesis. J. Biol. Chem., 2012, 287(28), 23527-23536.
[http://dx.doi.org/10.1074/jbc.M111.324673] [PMID: 22593578 ]
[49]
Inubushi, T.; Kawazoe, A.; Miyauchi, M.; Yanagisawa, S.; Subarnbhesaj, A.; Chanbora, C.; Ayuningtyas, N.F.; Ishikado, A.; Tanaka, E.; Takata, T. Lactoferrin inhibits infection-related osteoclastogenesis without interrupting compressive force-related osteoclastogenesis. Arch. Oral Biol., 2014, 59(2), 226-232.
[http://dx.doi.org/10.1016/j.archoralbio.2013.11.002] [PMID: 24370195 ]
[50]
Guo, H.Y.; Jiang, L.; Ibrahim, S.A.; Zhang, L.; Zhang, H.; Zhang, M.; Ren, F.Z. Orally administered lactoferrin preserves bone mass and microarchitecture in ovariectomized rats. J. Nutr., 2009, 139(5), 958-964.
[http://dx.doi.org/10.3945/jn.108.100586] [PMID: 19321577]
[51]
Blais, A.; Malet, A.; Mikogami, T.; Martin-Rouas, C.; Tomé, D. Oral bovine lactoferrin improves bone status of ovariectomized mice. Am. J. Physiol. Endocrinol. Metab., 2009, 296(6), E1281-E1288.
[http://dx.doi.org/10.1152/ajpendo.90938.2008] [PMID: 19336659 ]
[52]
Bharadwaj, S.; Naidu, T.A.; Betageri, G.V.; Prasadarao, N.V.; Naidu, A.S. Inflammatory responses improve with milk ribonuclease-enriched lactoferrin supplementation in postmenopausal women. Inflamm. Res., 2010, 59(11), 971-978.
[http://dx.doi.org/10.1007/s00011-010-0211-7] [PMID: 20473630 ]
[53]
Ieni, A.; Barresi, V.; Grosso, M.; Rosa, M.A.; Tuccari, G. Immunolocalization of lactoferrin in cartilage-forming neoplasms. J. Orthop. Sci., 2009, 14(6), 732-737.
[http://dx.doi.org/10.1007/s00776-009-1396-x] [PMID: 19997820 ]
[54]
Antonio, I.; Valeria, B.; Maddalena, G.; Giovanni, T. Immunohistochemical evidence of lactoferrin in human embryo-fetal bone and cartilage tissues. Cell Biol. Int., 2010, 34(8), 845-849.
[http://dx.doi.org/10.1042/CBI20090358] [PMID: 20443779 ]
[55]
Ieni, A.; Barresi, V.; Grosso, M.; Speciale, G.; Rosa, M.A.; Tuccari, G. Does lactoferrin behave as an immunohistochemical oncofetal marker in bone and cartilage human neoplasms? Pathol. Oncol. Res., 2011, 17(2), 287-293.
[http://dx.doi.org/10.1007/s12253-010-9311-5] [PMID: 20972893 ]
[56]
Malet, A.; Bournaud, E.; Lan, A.; Mikogami, T.; Tomé, D.; Blais, A. Bovine lactoferrin improves bone status of ovariectomized mice via immune function modulation. Bone, 2011, 48(5), 1028-1035.
[http://dx.doi.org/10.1016/j.bone.2011.02.002] [PMID: 21303707 ]
[57]
Amini, A.A.; Nair, L.S. Lactoferrin: a biologically active molecule for bone regeneration. Curr. Med. Chem., 2011, 18(8), 1220-1229.
[http://dx.doi.org/10.2174/092986711795029744] [PMID: 21291364 ]
[58]
Hou, J.M.; Xue, Y.; Lin, Q.M. Bovine lactoferrin improves bone mass and microstructure in ovariectomized rats via OPG/RANKL/RANK pathway. Acta Pharmacol. Sin., 2012, 33(10), 1277-1284.
[http://dx.doi.org/10.1038/aps.2012.83] [PMID: 22902986]
[59]
Yoshimaki, T.; Sato, S.; Tsunori, K.; Shino, H.; Iguchi, S.; Arai, Y.; Ito, K.; Ogiso, B. Bone regeneration with systemic administration of lactoferrin in non-critical-sized rat calvarial bone defects. J. Oral Sci., 2013, 55(4), 343-348.
[http://dx.doi.org/10.2334/josnusd.55.343] [PMID: 24351923 ]
[60]
Li, W.; Zhu, S.; Hu, J. Bone regeneration is promoted by orally administered bovine lactoferrin in a rabbit tibial distraction osteogenesis model. Clin. Orthop. Relat. Res., 2015, 473(7), 2383-2393.
[http://dx.doi.org/10.1007/s11999-015-4270-5] [PMID: 25822454 ]
[61]
Takaoka, R.; Hikasa, Y.; Hayashi, K.; Tabata, Y. Bone regeneration by lactoferrin released from a gelatin hydrogel. J. Biomater. Sci. Polym. Ed., 2011, 22(12), 1581-1589.
[http://dx.doi.org/10.1163/092050610X517095] [PMID: 20663279 ]
[62]
Görmez, U.; Kürkcü, M.E.; Benlidayi, M.; Ulubayram, K.; Sertdemir, Y.; Dağlioğlu, K. Effects of bovine lactoferrin in surgically created bone defects on bone regeneration around implants. J. Oral Sci., 2015, 57(1), 7-15.
[http://dx.doi.org/10.2334/josnusd.57.7] [PMID: 25807903]
[63]
Paknejad, M.; Rokn, A.R.; Yaraghi, A.A.S.; Elhami, F.; Kharazifard, M.J.; Moslemi, N. Histologic and histomorphometric evaluation of the effect of lactoferrin combined with anorganic bovine bone on healing of experimentally induced bony defects on rabbit calvaria. Dent. Res. J. (Isfahan), 2012, 9(Suppl. 1), S75-S80.
[PMID: 23814566 ]
[64]
Gao, R.; Watson, M.; Callon, K.E.; Tuari, D.; Dray, M.; Naot, D.; Amirapu, S.; Munro, J.T.; Cornish, J.; Musson, D.S. Local application of lactoferrin promotes bone regeneration in a rat critical-sized calvarial defect model as demonstrated by micro-CT and histological analysis. J. Tissue Eng. Regen. Med., 2018, 12(1), e620-e626.
[http://dx.doi.org/10.1002/term.2348] [PMID: 27860377 ]
[65]
Saki, A.A.; Mahmoudi, H. Effects of in ovo injection of bovine lactoferrin before incubation in layer breeder eggs on tibia measurements and performance of laying hens. Animal, 2015, 9(11), 1813-1819.
[http://dx.doi.org/10.1017/S1751731115001093] [PMID: 26178907 ]
[66]
Li, Q.; Zhao, J.; Hu, W.; Wang, J.; Yu, T.; Dai, Y.; Li, N. Effects of recombinant human lactoferrin on osteoblast growth and bone status in piglets. Anim. Biotechnol., 2018, 29(2), 90-99.
[http://dx.doi.org/10.1080/10495398.2017.1313269] [PMID: 28494220 ]
[67]
Calvani, F.; Cutone, A.; Lepanto, M.S.; Rosa, L.; Valentini, V.; Valenti, P. Efficacy of bovine lactoferrin in the post-surgical treatment of patients suffering from bisphosphonate-related osteonecrosis of the jaws: an open-label study. Biometals, 2018, 31(3), 445-455.
[http://dx.doi.org/10.1007/s10534-018-0081-y] [PMID: 29435826 ]
[68]
Cornish, J.; Palmano, K.; Callon, K.E.; Watson, M.; Lin, J.M.; Valenti, P.; Naot, D.; Grey, A.B.; Reid, I.R. Lactoferrin and bone; structure-activity relationships. Biochem. Cell Biol., 2006, 84(3), 297-302.
[http://dx.doi.org/10.1139/o06-057] [PMID: 16936800 ]
[69]
Amini, A.A.; Nair, L.S. Evaluation of the bioactivity of recombinant human lactoferrins toward murine osteoblast-like cells for bone tissue engineering. Tissue Eng. Part A, 2013, 19(9-10), 1047-1055.
[http://dx.doi.org/10.1089/ten.tea.2012.0227] [PMID: 23270517 ]
[70]
Wang, X.Y.; Guo, H.Y.; Zhang, W.; Wen, P.C.; Zhang, H.; Guo, Z.R.; Ren, F.Z. Effect of iron saturation level of lactoferrin on osteogenic activity in vitro and in vivo. J. Dairy Sci., 2013, 96(1), 33-39.
[http://dx.doi.org/10.3168/jds.2012-5692] [PMID: 23164231 ]
[71]
Baker, H.M.; Baker, E.N. Lactoferrin and iron: structural and dynamic aspects of binding and release. Biometals, 2004, 17(3), 209-216.
[http://dx.doi.org/10.1023/B:BIOM.0000027694.40260.70] [PMID: 15222467 ]
[72]
Yao, X.D.; Bunt, C.; Cornish, J.; Quek, S.Y.; Wen, J.Y. Oral delivery of lactoferrin: a review. Int. J. Pept. Res. Ther., 2013, 19(2), 125-134.
[http://dx.doi.org/10.1007/s10989-012-9326-8]
[73]
Samarasinghe, R.M.; Kanwar, R.K.; Kanwar, J.R. The effect of oral administration of iron saturated-bovine lactoferrin encapsulated chitosan-nanocarriers on osteoarthritis. Biomaterials, 2014, 35(26), 7522-7534.
[http://dx.doi.org/10.1016/j.biomaterials.2014.04.109] [PMID: 24933511 ]
[74]
Giansanti, F.; Panella, G.; Leboffe, L.; Antonini, G. Lactoferrin from milk: nutraceutical and pharmacological properties. Pharmaceuticals (Basel), 2016, 9(4), 61.
[http://dx.doi.org/10.3390/ph9040061] [PMID: 27690059 ]
[75]
Takayama, Y.; Mizumachi, K. Effect of lactoferrin-embedded collagen membrane on osteogenic differentiation of human osteoblast-like cells. J. Biosci. Bioeng., 2009, 107(2), 191-195.
[http://dx.doi.org/10.1016/j.jbiosc.2008.09.018] [PMID: 19217559]
[76]
Kim, S.E.; Yun, Y.P.; Shim, K.S.; Park, K.; Choi, S.W.; Suh, D.H. Effect of lactoferrin-impregnated porous poly(lactide-co-glycolide) (PLGA) microspheres on osteogenic differentiation of rabbit adipose-derived stem cells (rADSCs). Colloids Surf. B Biointerfaces, 2014, 122, 457-464.
[http://dx.doi.org/10.1016/j.colsurfb.2014.06.057] [PMID: 25096719 ]
[77]
James, E.N.; Nair, L.S. Development and characterization of lactoferrin loaded poly(epsilon-caprolactone) nanofibers. J. Biomed. Nanotechnol., 2014, 10(3), 500-507.
[http://dx.doi.org/10.1166/jbn.2014.1717] [PMID: 24730245 ]
[78]
Vandrovcova, M.; Douglas, T.E.; Heinemann, S.; Scharnweber, D.; Dubruel, P.; Bacakova, L. Collagen-lactoferrin fibrillar coatings enhance osteoblast proliferation and differentiation. J. Biomed. Mater. Res. A, 2015, 103(2), 525-533.
[http://dx.doi.org/10.1002/jbm.a.35199] [PMID: 24737729 ]
[79]
Kim, S.E.; Yun, Y.P.; Lee, J.Y.; Park, K.; Suh, D.H. Osteoblast activity of MG-63 cells is enhanced by growth on a lactoferrin-immobilized titanium substrate. Colloids Surf. B Biointerfaces, 2014, 123, 191-198.
[http://dx.doi.org/10.1016/j.colsurfb.2014.09.014] [PMID: 25277288 ]
[80]
Wennerberg, A.; Albrektsson, T. Effects of titanium surface topography on bone integration: a systematic review. Clin. Oral Implants Res., 2009, 20(Suppl. 4), 172-184.
[http://dx.doi.org/10.1111/j.1600-0501.2009.01775.x] [PMID: 19663964 ]
[81]
Cavalcanti, Y.W.; Soare, R.V.; Leite Assis, M.A.; Zenóbio, E.G.; Girundi, F.M. Titanium surface roughing treatments contribute to higher interaction with salivary proteins MG2 and lactoferrin. J. Contemp. Dent. Pract., 2015, 16(2), 141-146.
[http://dx.doi.org/10.5005/jp-journals-10024-1651] [PMID: 25906806]
[82]
Kazek-Kesik, A.; Pietryga, K.; Basiaga, M.; Blacha-Grzechnik, A.; Dercz, G.; Kalemba-Rec, I.; Pamula, E.; Simka, W. Lactoferrin and collagen type I as components of composite formed on titanium alloys for bone replacement. Surf. Coat. Tech., 2017, 328, 1-12.
[http://dx.doi.org/10.1016/j.surfcoat.2017.08.022]
[83]
Nocerino, N.; Fulgione, A.; Iannaccone, M.; Tomasetta, L.; Ianniello, F.; Martora, F.; Lelli, M.; Roveri, N.; Capuano, F.; Capparelli, R. Biological activity of lactoferrin-functionalized biomimetic hydroxyapatite nanocrystals. Int. J. Nanomedicine, 2014, 9, 1175-1184.
[PMID: 24623976]
[84]
Montesi, M.; Panseri, S.; Iafisco, M.; Adamiano, A.; Tampieri, A. Effect of hydroxyapatite nanocrystals functionalized with lactoferrin in osteogenic differentiation of mesenchymal stem cells. J. Biomed. Mater. Res. A, 2015, 103(1), 224-234.
[http://dx.doi.org/10.1002/jbm.a.35170] [PMID: 24639083 ]
[85]
Montesi, M.; Panseri, S.; Iafisco, M.; Adamiano, A.; Tampieri, A. Coupling hydroxyapatite nanocrystals with lactoferrin as a promising strategy to fine regulate bone homeostasis. PLoS One, 2015, 10(7)e0132633
[http://dx.doi.org/10.1371/journal.pone.0132633] [PMID: 26148296 ]
[86]
Kim, S.E.; Lee, D.W.; Yun, Y.P.; Shim, K.S.; Jeon, D.I.; Rhee, J.K.; Kim, H.J.; Park, K. Heparin-immobilized hydroxyapatite nanoparticles as a lactoferrin delivery system for improving osteogenic differentiation of adipose-derived stem cells. Biomed. Mater., 2016, 11(2) 025004
[http://dx.doi.org/10.1088/1748-6041/11/2/025004] [PMID: 26963891]
[87]
Shi, P.; Wang, Q.; Yu, C.; Fan, F.; Liu, M.; Tu, M.; Lu, W.; Du, M. Hydroxyapatite nanorod and microsphere functionalized with bioactive lactoferrin as a new biomaterial for enhancement bone regeneration. Colloids Surf. B Biointerfaces, 2017, 155, 477-486.
[http://dx.doi.org/10.1016/j.colsurfb.2017.04.042] [PMID: 28472751 ]
[88]
Amini, A.A.; Kan, H.M.; Cui, Z.; Maye, P.; Nair, L.S. Enzymatically cross-linked bovine lactoferrin as injectable hydrogel for cell delivery. Tissue Eng. Part A, 2014, 20(21-22), 2830-2839.
[http://dx.doi.org/10.1089/ten.tea.2013.0506] [PMID: 24802947 ]
[89]
Palmano, K.P.; Ramos, R.; Watson, M.; Callon, K.E.; Cornish, J. Survival and bone-active properties of bovine lactoferrin supplemented into stirred yoghurt. Int. Dairy J., 2011, 21(7), 477-483.
[http://dx.doi.org/10.1016/j.idairyj.2011.02.006]
[90]
Banerjee, R. Liposomes: applications in medicine. J. Biomater. Appl., 2001, 16(1), 3-21.
[http://dx.doi.org/10.1106/RA7U-1V9C-RV7C-8QXL] [PMID: 11475357]
[91]
Torchilin, V.P. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov., 2005, 4(2), 145-160.
[http://dx.doi.org/10.1038/nrd1632] [PMID: 15688077]
[92]
Immordino, M.L.; Dosio, F.; Cattel, L. Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential. Int. J. Nanomedicine, 2006, 1(3), 297-315.
[PMID: 17717971 ]
[93]
Gregoriadis, G., Ed.; Liposome technology, 3rd ed; Informa Healthcare USA, Inc.: New York, USA, 2007.
[94]
Fenske, D.B.; Chonn, A.; Cullis, P.R. Liposomal nanomedicines: an emerging field. Toxicol. Pathol., 2008, 36(1), 21-29.
[http://dx.doi.org/10.1177/0192623307310960] [PMID: 18337218 ]
[95]
Allen, T.M.; Cullis, P.R. Liposomal drug delivery systems: from concept to clinical applications. Adv. Drug Deliv. Rev., 2013, 65(1), 36-48.
[http://dx.doi.org/10.1016/j.addr.2012.09.037] [PMID: 23036225 ]
[96]
Trif, M.; Craciunescu, O. Liposome as efficient system for intracellular delivery of bioactive molecules in: Nanotechnology and Functional Foods: Effective Delivery of Bioactive Ingredients; Sabliov, C.M.; Chen, H; Yada, R.Y., Ed.; John Wiley & Sons Inc: UK, 2015, pp. 191-213.
[http://dx.doi.org/10.1002/9781118462157.ch12]
[97]
Trif, M.; Guillen, C.; Vaughan, D.M.; Telfer, J.M.; Brewer, J.M.; Roseanu, A.; Brock, J.H. Liposomes as possible carriers for lactoferrin in the local treatment of inflammatory diseases. Exp. Biol. Med. (Maywood), 2001, 226(6), 559-564.
[http://dx.doi.org/10.1177/153537020122600608] [PMID: 11395926 ]
[98]
Trif, M.; Roseanu, A.; Brock, J.H.; Brewer, J.M. Designing lipid nanostructures for local delivery of biologically active macromolecules. J. Liposome Res., 2007, 17(3-4), 237-248.
[http://dx.doi.org/10.1080/08982100701530027] [PMID: 18027244]
[99]
Zhang, Z.; Huang, G. Micro- and nano-carrier mediated intra-articular drug delivery systems for the treatment of osteoarthritis. Journal of Nanotechnology., 2012.
[100]
Moisei, M.; Craciunescu, O.; Moldovan, L.; Roseanu, A.; Trif, M. Lipid nanostructures containing atorvastatin decrease lipopolysaccharide-induced inflammation in macrophages. J. Nanosci. Nanotechnol., 2017, 17(7), 4631-4637.
[http://dx.doi.org/10.1166/jnn.2017.13745]
[101]
Monteiro, N.; Martins, A.; Reis, R.L.; Neves, N.M. Liposomes in tissue engineering and regenerative medicine. J. R. Soc. Interface, 2014, 11(101)20140459
[http://dx.doi.org/10.1098/rsif.2014.0459] [PMID: 25401172 ]
[102]
Mountziaris, P.M.; Mikos, A.G. Modulation of the inflammatory response for enhanced bone tissue regeneration. Tissue Eng. Part B Rev., 2008, 14(2), 179-186.
[http://dx.doi.org/10.1089/ten.teb.2008.0038] [PMID: 18544015 ]
[103]
Mountziaris, P.M.; Spicer, P.P.; Kasper, F.K.; Mikos, A.G. Harnessing and modulating inflammation in strategies for bone regeneration. Tissue Eng. Part B Rev., 2011, 17(6), 393-402.
[http://dx.doi.org/10.1089/ten.teb.2011.0182] [PMID: 21615330 ]
[104]
Yao, X.; Bunt, C.; Cornish, J.; Quek, S.Y.; Wen, J. Preparation, optimization and characterization of bovine lactoferrin-loaded liposomes and solid lipid particles modified by hydrophilic polymers using factorial design. Chem. Biol. Drug Des., 2014, 83(5), 560-575.
[http://dx.doi.org/10.1111/cbdd.12269] [PMID: 24325576 ]
[105]
Ishikado, A.; Imanaka, H.; Takeuchi, T.; Harada, E.; Makino, T. Liposomalization of lactoferrin enhanced it’s anti-inflammatory effects via oral administration. Biol. Pharm. Bull., 2005, 28(9), 1717-1721.
[http://dx.doi.org/10.1248/bpb.28.1717] [PMID: 16141546 ]
[106]
Ishikado, A.; Imanaka, H.; Suido, H.; Makino, T. Osteoclast growth inhibitor, oral composition, and preventive or therapeutic agent for bone diseases, containing liposome - encapsulated lactoferrin. United States patent application US 12/084,151 2009.
[107]
Ishikado, A.; Uesaki, S.; Suido, H.; Nomura, Y.; Sumikawa, K.; Maeda, M.; Miyauchi, M.; Takata, T.; Makino, T. Human trial of liposomal lactoferrin supplementation for periodontal disease. Biol. Pharm. Bull., 2010, 33(10), 1758-1762.
[http://dx.doi.org/10.1248/bpb.33.1758] [PMID: 20930389 ]
[108]
Kawazoe, A.; Inubushi, T.; Miyauchi, M.; Ishikado, A.; Tanaka, E.; Tanne, K.; Takata, T. Orally administered liposomal lactoferrin inhibits inflammation-related bone breakdown without interrupting orthodontic tooth movement. J. Periodontol., 2013, 84(10), 1454-1462.
[http://dx.doi.org/10.1902/jop.2012.120508] [PMID: 23136974]


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VOLUME: 27
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Year: 2020
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DOI: 10.2174/0929867326666190503121546
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