Octacalcium phosphate crystals including a higher density dislocation improve its materials osteogenecity

[1] K. Yokoyama, M. Tomita, J. Sakai, Hydrogen embrittlement behavior induced by dynamic martensite transformation of Ni–Ti superelastic alloy, Acta Mater. 57 (2009) 1875–1885, doi:10.1016/j.actamat.2008.12.030.

[2] E. Bres, J. Barry, J. Hutchison, A structural basis for the carious dissolution of the apatite crystals of human tooth enamel, Ultramicroscopy 12 (1983) 367– 371, doi:10.1016/0304-3991(83)90250- 4.

[3] A. Matsugaki, G. Aramoto, T. Nakano, The alignment of MC3T3-E1 osteoblasts on steps of slip traces introduced by dislocation motion, Biomaterials 33 (2012) 7327–7335, doi:10.1016/j.biomaterials.2012.06.022.

[4] T. Kawai, S. Kamakura, K. Matsui, M. Fukuda, H. Takano, M. Iino, S. Ishikawa, H. Kawana, T. Soma, E. Imamura, H. Kizu, A. Michibata, I. Asahina, K. Miura, N. Nakamura, T. Kibe, O. Suzuki, T. Takahashi, Clinical study of octacalcium phosphate and collagen composite in oral and maxillofacial surgery, J. Tissue Eng. 11 (2020) 2041731419896449, doi:10.1177/2041731419896449.

[5] O. Suzuki, S. Kamakura, T. Katagiri, M. Nakamura, B. Zhao, Y. Honda, R. Kamijo, Bone formation enhanced by implanted octacalcium phosphate involving con- version into Ca-deficient hydroxyapatite, Biomaterials 27 (2006) 2671–2681, doi:10.1016/j.biomaterials.2005.12.004.

[6] O. Suzuki, M. Nakamura, Y. Miyasaka, M. Kagayama, M. Sakurai, Bone forma- tion on synthetic precursors of hydroxyapatite, Tohoku J. Exp. Med. 164 (1991) 37–50, doi:10.1620/tjem.164.37.

[7] H. Imaizumi, M. Sakurai, O. Kashimoto, T. Kikawa, O. Suzuki, Comparative study on osteoconductivity by synthetic octacalcium phosphate and sintered hydroxyapatite in rabbit bone marrow, Calcif. Tissue Int. 78 (2006) 45–54, doi:10.1007/s00223-005-0170-0.

[8] N. Miyatake, K.N. Kishimoto, T. Anada, H. Imaizumi, E. Itoi, O. Suzuki, Effect of partial hydrolysis of octacalcium phosphate on its osteoconductive characteris- tics, Biomaterials 30 (2009) 1005–1014, doi:10.1016/j.biomaterials.2008.10.058.

[9] S. Saito, R. Hamai, Y. Shiwaku, T. Hasegawa, S. Sakai, K. Tsuchiya, Y. Sai, R. Iwama, N. Amizuka, T. Takahashi, O. Suzuki, Involvement of distant octa- calcium phosphate scaffolds in enhancing early differentiation of osteocytes during bone regeneration, Acta Biomater. 129 (2021) 309–322, doi:10.1016/j. actbio.2021.05.017.

[10] O. Suzuki, S. Kamakura, T. Katagiri, Surface chemistry and biological responses to synthetic octacalcium phosphate, J. Biomed. Mater. Res. Part B 77 (2006) 201–212, doi:10.1002/jbm.b.30407.

[11] R. Nishikawa, T. Anada, R. Ishiko-Uzuka, O. Suzuki, Osteoblastic differentiation of stromal ST-2 cells from octacalcium phosphate exposure via p38 signaling pathway, Dent. Mater. J. 33 (2014) 242–251, doi:10.4012/dmj.2013-226.

[12] M. Takami, A. Mochizuki, A. Yamada, K. Tachi, B. Zhao, Y. Miyamoto, T. Anada, Y. Honda, T. Inoue, M. Nakamura, O. Suzuki, R. Kamijo, Osteoclast differenti- ation induced by synthetic octacalcium phosphate through receptor activator of NF-κB ligand expression in osteoblasts, Tissue Eng. Part A 15 (2009) 3991– 4000, doi:10.1089/ten.TEA.2009.0065.

[13] Y. Sai, Y. Shiwaku, T. Anada, K. Tsuchiya, T. Takahashi, O. Suzuki, Capacity of oc- tacalcium phosphate to promote osteoblastic differentiation toward osteocytes in vitro, Acta Biomater. 69 (2018) 362–371, doi:10.1016/j.actbio.2018.01.026.

[14] J.L. Meyer, E.D. Eanes, A thermodynamic analysis of the secondary transition in the spontaneous precipitation of calcium phosphate, Calcif. Tissue Res. 25 (1978) 209–216, doi:10.1007/bf02010771.

[15] W.E. Brown, Crystal growth of bone mineral, Clin. Orthop. Relat. Res. 44 (1966) 205–220.

[16] W.E. Brown, J.P. Smith, J.R. Lehr, A.W. Frazier, Octacalcium phosphate and hydroxyapatite: crystallographic and chemical relations between octacalcium phosphate and hydroxyapatite, Nature 196 (1962) 1050–1055, doi:10.1038/ 1961050a0.

[17] M. Mathew, W.E. Brown, L.W. Schroeder, B. Dickens, Crystal struc- ture of octacalcium bis(hydrogenphosphate) tetrakis(phosphate)pentahydrate, Ca8 (HPO4 )2 (PO4 )4 ·5H2 O, J. Crystallogr. Spectrosc. Res. 18 (1988) 235–250, doi:10.1007/BF01194315.

[18] D.R. Simpson, Problems of the composition and structure of the bone minerals, Clin. Orthop. Relat. Res. 86 (1972) 260–286, doi:10.1097/ 00003086-197207000-00039.

[19] C. Rey, C. Combes, What bridges mineral platelets of bone? BoneKEy Rep. 3 (2014) 1–2, doi:10.1038/bonekey.2014.81.

[20] P. Simon, D. Grüner, H. Worch, W. Pompe, H. Lichte, T. El Khassawna, C. Heiss, S. Wenisch, R. Kniep, First evidence of octacalcium phosphate@ osteocalcin nanocomplex as skeletal bone component directing collagen triple–helix nanofibril mineralization, Sci. Rep. 8 (2018) 13696, doi:10.1038/s41598-018-31983- 5.

[21] O. Suzuki, H. Yagishita, T. Amano, T. Aoba, Reversible structural changes of oc- tacalcium phosphate and labile acid phosphate, J. Dent. Res. 74 (1995) 1764– 1769, doi:10.1177/00220345950740110801.

[22] W.J. Habraken, J. Tao, L.J. Brylka, H. Friedrich, L. Bertinetti, A.S. Schenk, A. Verch, V. Dmitrovic, P.H. Bomans, P.M. Frederik, J. Laven, P. van der Schoot, B. Aichmayer, G.de With, J.J. DeYoreo, N.A.J.M. Sommerdijk, Ion-association complexes unite classical and non-classical theories for the biomimetic nu-cleation of calcium phosphate, Nat. Commun. 4 (2013) 1507, doi:10.1038/ ncomms2490.

[23] W.E. Brown, J.R. Lehr, J.P. Smith, A.W. Frazier, Crystallography of octacalcium phosphate, J. Am. Chem. Soc. 79 (1957) 5318–5319, doi:10.1021/ja01576a068.

[24] H. Newsely, Darstellung von “Oktacalciumphosphat”(Tetracalcium- hydrogentrisphosphat) durch homogene kristallisation, Monatsh. Chem. 91 (1960) 1020–1023, doi:10.1007/BF00899825.

[25] E. Hayek, Die mineralsubstanz der knochen, Klin. Wochenschr. 45 (1967) 857–863, doi:10.1007/BF01745681.

[26] Y. Liu, R. Shelton, J. Barralet, Homogeneous octacalcium phosphate precipita- tion: effect of temperature and pH, Key Eng. Mater. 254-256 (2003) 79–82, doi:10.4028/www.scientific.net/KEM.254-256.79.

[27] M. Iijima, H. Kamemizu, N. Wakamatsu, T. Goto, Y. Doi, Y. Moriwaki, Effects of Ca addition on the formation of octacalcium phosphate and apatite in solu- tion at pH 7.4 and at 37°C, J. Cryst. Growth 193 (1998) 182–188, doi:10.1016/S0022-0248(98)00455-2.

[28] A. Bigi, B. Bracci, S. Panzavolta, M. Iliescu, M. Plouet-Richard, J. Werckmann, D. Cam, Morphological and structural modifications of octacalcium phosphate induced by poly-l-aspartate, Cryst. Growth Des. 4 (2004) 141–146, doi:10.1021/ cg034078d.

[29] J. Moradian-Oldak, M. Iijima, N. Bouropoulos, H.B. Wen, Assembly of amelogenin proteolytic products and control of octacalcium phosphate crystal morphology, Connect. Tissue Res. 44 (2003) 58–64, doi:10.1080/03008200390152106.

[30] K. Tsuchiya, R. Hamai, S. Sakai, O. Suzuki, Comparative analysis of bovine serum albumin adsorption onto octacalcium phosphate crystals prepared us- ing different methods, Dent. Mater. J. 39 (2020) 883–891, doi:10.4012/dmj. 2019-250.

[31] T. Handa, T. Anada, Y. Honda, H. Yamazaki, K. Kobayashi, N. Kanda, S. Ka- makura, S. Echigo, O. Suzuki, The effect of an octacalcium phosphate co- precipitated gelatin composite on the repair of critical-sized rat calvarial de- fects, Acta Biomater. 8 (2012) 1190–1200, doi:10.1016/j.actbio.2011.12.002.

[32] S. Chiba, T. Anada, K. Suzuki, K. Saito, Y. Shiwaku, N. Miyatake, K. Baba, H. Imaizumi, M. Hosaka, E. Itoi, O. Suzuki, Effect of resorption rate and osteo- conductivity of biodegradable calcium phosphate materials on the acquisition of natural bone strength in the repaired bone, J. Biomed. Mater. Res. Part A 104 (2016) 2833–2842, doi:10.1002/jbm.a.35828.

[33] R. Ishiko-Uzuka, T. Anada, K. Kobayashi, T. Kawai, Y. Tanuma, K. Sasaki, O. Suzuki, Oriented bone regenerative capacity of octacalcium phos- phate/gelatin composites obtained through two-step crystal preparation method, J. Biomed. Mater. Res. Part B 105 (2017) 1029–1039, doi:10.1002/jbm. b.33640.

[34] S. Sakai, T. Anada, K. Tsuchiya, H. Yamazaki, H.C. Margolis, O. Suzuki, Compar-ative study on the resorbability and dissolution behavior of octacalcium phos- phate, β-tricalcium phosphate, and hydroxyapatite under physiological condi- tions, Dent. Mater. J. 35 (2016) 216–224, doi:10.4012/dmj.2015-255.

[35] T. Kokubo, H. Takadama, How useful is SBF in predicting in vivo bone bioactiv- ity? Biomaterials 27 (2006) 2907–2915, doi:10.1016/j.biomaterials.2006.01.017.

[36] K. Baba, Y. Shiwaku, R. Hamai, Y. Mori, T. Anada, K. Tsuchiya, I. Oizumi, N. Miy- atake, E. Itoi, O. Suzuki, Chemical stability-sensitive osteoconductive perfor- mance of octacalcium phosphate bone substitute in an ovariectomized rat tibia defect, ACS Appl. Bio Mater. 3 (2020) 1444–1458, doi:10.1021/acsabm.9b01091.

[37] T. Sato, T. Anada, R. Hamai, Y. Shiwaku, K. Tsuchiya, S. Sakai, K. Baba, K. Sasaki, O. Suzuki, Culture of hybrid spheroids composed of calcium phosphate ma- terials and mesenchymal stem cells on an oxygen-permeable culture device to predict in vivo bone forming capability, Acta Biomater. 88 (2019) 477–490, doi:10.1016/j.actbio.2019.03.001.

[38] T. Anada, J. Fukuda, Y. Sai, O. Suzuki, An oxygen-permeable spheroid culture system for the prevention of central hypoxia and necrosis of spheroids, Bio- materials 33 (2012) 8430–8441, doi:10.1016/j.biomaterials.2012.08.040.

[39] M. Wakasa, K. Nakanishi, K. Manago, T. Isobe, Y. Eshita, M. Okamoto, T. Isshiki, Fine structure of tooth enamel in the yellowing human teeth: SEM and HRTEM studies, Microsc. Res. Tech. 79 (2016) 14–22, doi:10.1002/jemt.22600.

[40] Q. Wang, S. Ri, H. Tsuda, M. Kodera, K. Suguro, N. Miyashita, Visualization and automatic detection of defect distribution in GaN atomic structure from sam- pling Moiré phase, Nanotechnology 28 (2017) 455704, doi:10.1088/1361-6528/ aa8d83.

[41] D. Hull, D.J. Bacon, Introduction to Dislocations, 5th ed., Butterworth-Heine- mann, Oxford, 2011.

[42] A.E. Porter, S.M. Best, W. Bonfield, Ultrastructural comparison of hydroxya- patite and silicon-substituted hydroxyapatite for biomedical applications, J. Biomed. Mater. Res. Part A 68A (2004) 133–141, doi:10.1002/jbm.a.20064.

[43] K. Okuyama, K. Miyama, K. Mizuno, H.P. Bächinger, Crystal structure of (Gly- Pro-Hyp) 9: implications for the collagen molecular model, Biopolymers 97 (2012) 607–616, doi:10.1002/bip.22048.

[44] L. Wang, G.H. Nancollas, Calcium orthophosphates: crystallization and dissolu- tion, Chem. Rev. 108 (2008) 4628–4669, doi:10.1021/cr0782574.

[45] W.E. Brown, M. Mathew, M.S. Tung, Crystal-chemistry of octacalcium phos- phate, Prog. Cryst. Growth Charact. 4 (1981) 59–87, doi:10.1016/0146-3535(81)90048-4.

[46] N. Eidelman, L.C. Chow, W.E. Brown, Calcium phosphate saturation levels in ul- trafiltered serum, Calcif. Tissue Int. 40 (1987) 71–78, doi:10.1007/BF02555708.

[47] D.G.A. Nelson, J.D. McLean, High-resolution electron microscopy of octacalcium phosphate and its hydrolysis products, Calcif. Tissue Int. 36 (1984) 219–232, doi:10.1007/BF02405321.

[48] M. Iijima, H. Kamemizu, N. Wakamatsu, T. Goto, Y. Doi, Y. Moriwaki, Transition of octacalcium phosphate to hydroxyapatite in solution at pH 7.4 and 37°C, J. Cryst. Growth 181 (1997) 70–78, doi:10.1016/S0022-0248(97)00230-3.

[49] N. Ito, M. Kamitakahara, M. Yoshimura, K. Ioku, Importance of nucleation in transformation of octacalcium phosphate to hydroxyapatite, Mater. Sci. Eng. C 40 (2014) 121–126, doi:10.1016/j.msec.2014.03.034.

[50] R. Tang, W. Wu, M. Haas, G.H. Nancollas, Kinetics of dissolution of β-tricalcium phosphate, Langmuir 17 (2001) 3480–3485, doi:10.1021/la001730n.

[51] M. Ohara, R.C. Reid, Modeling Crystal Growth Rates from Solution, Pren- tice-Hall, Englewood Cliffs, 1973.

[52] H.H. Teng, Controls by saturation state on etch pit formation during cal- cite dissolution, Geochim. Cosmochim. Acta 68 (2004) 253–262, doi:10.1016/ S0016-7037(03)00423-X.

[53] A.E. Blum, R.A. Yund, A.C. Lasaga, The effect of dislocation density on the dissolution rate of quartz, Geochim. Cosmochim. Acta 54 (1990) 283–297, doi:10.1016/0016-7037(90)90318- F.

[54] K.A. Gross, S. Saber-Samandari, K.S. Heemann, Evaluation of commercial im- plants with nanoindentation defines future development needs for hydroxya- patite coatings, J. Biomed. Mater. Res. Part B 93 (2010) 1–8, doi:10.1002/jbm.b. 31537.

[55] S. Saber-Samandari, K.A. Gross, Amorphous calcium phosphate offers improved crack resistance: a design feature from nature? Acta Biomater. 7 (2011) 4235– 4241, doi:10.1016/j.actbio.2011.06.048.

[56] S.S. Bhat, U.V. Waghmare, U. Ramamurty, First-principles study of structure, vibrational, and elastic properties of stoichiometric and calcium-deficient hy- droxyapatite, Cryst. Growth Des. 14 (2014) 3131–3141, doi:10.1021/cg5004269.

[57] K. Kobayashi, T. Anada, T. Handa, N. Kanda, M. Yoshinari, T. Takahashi, O. Suzuki, Osteoconductive property of a mechanical mixture of octacalcium phosphate and amorphous calcium phosphate, ACS Appl. Mater. Interfaces 6 (2014) 22602–22611, doi:10.1021/am5067139.

[58] T. Kurobane, Y. Shiwaku, T. Anada, R. Hamai, K. Tsuchiya, K. Baba, M. Iikubo, T. Takahashi, O. Suzuki, Angiogenesis involvement by octacalcium phosphate- gelatin composite-driven bone regeneration in rat calvaria critical-sized defect, Acta Biomater. 88 (2019) 514–526, doi:10.1016/j.actbio.2019.02.021.

[59] T. Nakano, K. Kaibara, Y. Tabata, N. Nagata, S. Enomoto, E. Marukawa, Y. Umakoshi, Unique alignment and texture of biological apatite crystallites in typical calcified tissues analyzed by microbeam X-ray diffractometer system, Bone 31 (2002) 479–487, doi:10.1016/S8756-3282(02)00850- 5.

[60] T. Ishimoto, T. Nakano, Y. Umakoshi, M. Yamamoto, Y. Tabata, Degree of biolog- ical apatite c-axis orientation rather than bone mineral density controls me- chanical function in bone regenerated using recombinant bone morphogenetic protein-2, J. Bone Miner. Res. 28 (2013) 1170–1179, doi:10.1002/jbmr.1825.

[61] O. Suzuki, H. Yagishita, M. Yamazaki, T. Aoba, Adsorption of bovine serum al- bumin onto octacalcium phosphate and its hydrolyzates, Cells Mater. 5 (1995) 45–54 https://digitalcommons.usu.edu/cellsandmaterials/vol5/iss1/4.

[62] K. Onuma, A. Ito, Cluster growth model for hydroxyapatite, Chem. Mater. 10 (1998) 3346–3351, doi:10.1021/cm980062c.

[63] M. Iijima, J. Moradian-Oldak, Control of octacalcium phosphate and apatite crystal growth by amelogenin matrices, J. Mater. Chem. 14 (2004) 2189–2199, doi:10.1039/B401961J.

[64] E. Davies, K.H. Müller, W.C. Wong, C.J. Pickard, D.G. Reid, J.N. Skepper, M.J. Duer, Citrate bridges between mineral platelets in bone, Proc. Natl. Acad. Sci. U S A. 111 (2014) E1354–E1363, doi:10.1073/pnas.1315080111.

[65] Y. Wang, S. Von Euw, F.M. Fernandes, S. Cassaignon, M. Selmane, G. Lau- rent, G. Pehau-Arnaudet, C. Coelho, L. Bonhomme-Coury, M.M. Giraud-Guille, F. Babonneau, T. Azais, N. Nassif, Water-mediated structuring of bone apatite, Nat. Mater. 12 (2013) 1144–1153, doi:10.1038/nmat3787.

[66] A. Lotsari, A.K. Rajasekharan, M. Halvarsson, M. Andersson, Transformation of amorphous calcium phosphate to bone-like apatite, Nat. Commun. 9 (2018) 4170, doi:10.1038/s41467-018-06570- x.

[67] S. Von Euw, Y. Wang, G. Laurent, C. Drouet, F. Babonneau, N. Nassif, T. Azais, Bone mineral: new insights into its chemical composition, Sci. Rep. 9 (2019) 8456, doi:10.1038/s41598-019-44620- 6.

[68] A. Dey, P.H. Bomans, F.A. Müller, J. Will, P.M. Frederik, G. de With, N.A.J.M. Sommerdijk, The role of prenucleation clusters in surface-induced cal- cium phosphate crystallization, Nat. Mater. 9 (2010) 1010–1014, doi:10.1038/ nmat2900.

[69] H. Zhu, D. Guo, L. Sun, H. Li, D.A.H. Hanaor, F. Schmidt, K. Xu, Nanostructural insights into the dissolution behavior of Sr-doped hydroxyapatite, J. Eur. Ce- ram. Soc. 38 (2018) 5554–5562, doi:10.1016/j.jeurceramsoc.2018.07.056.

[70] A.J. Nathanael, S.I. Hong, D. Mangalaraj, N. Ponpandian, P.C. Chen, Template- free growth of novel hydroxyapatite nanorings: formation mechanism and their enhanced functional properties, Cryst. Growth Des. 12 (2012) 3565–3574, doi:10.1021/cg3003959.

[71] I.S. Yahia, M. Shkir, S. AlFaify, V. Ganesh, H.Y. Zahran, M. Kilany, Facile microwave-assisted synthesis of Te-doped hydroxyapatite nanorods and nanosheets and their characterizations for bone cement applications, Mater. Sci. Eng. C 72 (2017) 472–480, doi:10.1016/j.msec.2016.11.074.