Цитология, 2023, T. 65, № 6, стр. 557-572

Обзор локальных клеточно-молекулярных процессов регенерации костной ткани, индуцированных кальцийфосфатными материалами

Л. А. Мирошниченко 1, Т. Ю. Полякова 2, Л. С. Литвинова 1*, И. А. Хлусов 1

1 Лаборатория клеточных и микрофлюидных технологий, Сибирский государственный медицинский университет
634050 Томск, Россия

2 Кафедра нормальной физиологии, Сибирский государственный медицинский университет
634050 Томск, Россия

* E-mail: larisalitvinova@yandex.ru

Поступила в редакцию 20.06.2023
После доработки 01.08.2023
Принята к публикации 04.08.2023

Аннотация

Одной из ведущих причин госпитализации, инвалидизации и смертности 50% женщин и 20% мужчин в возрастной группе старше 50 лет являются переломы костей и их осложнения, обусловленные заболеваниями опорно-двигательной системы. Активный поиск решения проблемы, связанной с ограничениями применения в клинике ауто-, алло- и ксенотрансплантатов, для замещения костных дефектов, инициировал развитие регенеративного подхода, основанного на постепенном замещении искусственного материала растущей костной тканью. Перспективными в этом отношении являются материалы на основе фосфатов кальция, выполняющие роль активного источника химических элементов (кальций, фосфор и др.), способные оптимизировать процесс срастания костного дефекта и обеспечить замену имплантата новой костной тканью. В представленном обзоре обобщены данные из литературы о локальной биологической активности, клетках-мишенях и молекулярных эффектах фосфатов кальция. Показано, что кальцийфосфатные материалы биосовместимы, способны адсорбировать регуляторные белки и клетки, оказывая влияние на их генетический и секреторный аппарат и запуская процесс дифференцировки МСК в остеогенном направлении. При этом успешная реализация локальных механизмов остеоинтеграции на границе раздела кость–имплантат снижает риск перипротезной инфекции и отторжения искусственных изделий. Дальнейшее изучение и использование кальцийфосфатных материалов позволит осуществить значительный прорыв в решении современных проблем регенерации костной ткани, связанный с точным (цифровым) биоинженерным подходом на основе аддитивных технологий и искусственного интеллекта.

Ключевые слова: кальцийфосфатные материалы, остеиндукция, остеогенные клетки, остеогенез, регенерация, мезенхимные стволовые клетки, клеточно-молекулярные механизмы

Список литературы

  1. Добринская М.Н. 2018. Влияние новых нанодисперсных допированных макро- и микроэлементами карбонат-фосфатов кальция на организм экспериментальных животных. Автореф. канд. дис. Екатеренбург. 20 с. (Dobrinskaya M.N. Influence of new nanosized calcium carbonate-phosphates doped with macro- and microelements on the body of experimental animals. Ph. D. Thesis. Yekaterinburg. 20 pp.).

  2. Дьячкова У.Д., Виговский М.А., Басалова Н. А., Григорьева О.А., Ефименко А.Ю. 2022. Внеклеточные везикулы МСК переключают фенотип макрофагов с провоспалительного на противовоспалительный. Гены и клетки. Т. 7. № 3. С. 81. (Dyachkova U.D., Vigovsky M.A., Basalova N.A., Grigorieva O.A., Efimenko A.Yu. 2022. MSC extracellular vesicles switch the macrophage phenotype from pro-inflammatory to anti-inflammatory. Genes and cells. V. 7. No 3. P. 81.)

  3. Иванюк Е.Э., Надеждин С.В., Покровская Л.А., Шуплецова В.В., Хазиахматова О.Г., Юрова К.А., Малащенко В.В., Литвинова Л.С., Хлусов И.А. 2018. Субпопуляции макрофагов и мезенхимные стволовые клетки в регуляции ремоделирования костной ткани. Цитология. Т. 60. № 4. С. 252. (Ivanyuk E.E., Nadezhdin S.V., Pokrovskaya L.A., Shupletsova V.V., Khaziakhmatova O.G., Yurova K.A., Malashchenko V.V., Litvinova L.S., Khlusov I.A. 2018. Macrophage subpopulations and mesenchymal stem cells in the regulation of bone tissue remodeling. Tsitologiya. V. 60. № 4. P. 252).

  4. Карлов А.В., Хлусов И.А. 2003. Зависимость процессов репаративного остеогенеза от поверхностных свойств имплантатов для остеосинтеза. Гений ортопедии № 3. С. 46. (Karlov A.V., Khlusov I.A. 2003. Dependence of the processes of reparative osteogenesis on the surface properties of implants for osteosynthesis. Orthopedic genius. № 3. P. 46).

  5. Корель А.В., Кузнецов С.Б. 2019. Тканеинженерные стратегии для восстановления дефектов костной ткани. Cовременное состояние вопроса. Межд. журн. прикладных и фунд. иссл. № 4. С. 228. (Korel A.V., Kuznetsov S.B. 2019. Tissue engineering strategies for the restoration of bone defects. The current state of the issue. International J. Applied Basic Res. № 4. Р. 228).

  6. Пичугин В.Ф., Сурменева М.A., Сурменев Р.А., Хлусов И.А., Эппле М. 2011. Исследование физико-химических и биологических свойств кальцийфосфатных покрытий, созданных методом ВЧ-магнетронного распыления кремнийзамещенного гидроксиапатита. Поверхность. Рентгеновские, синхротронные и нейтронные исследования. № 9. С. 54 (Pichugin V.F., Surmeneva M.A., Surmenev R.A., Khlusov I.A., Epple M. 2011. Study of physicochemical and biological properties of calcium phosphate coatings prepared by RF magnetron sputtering of silicon-substituted hydroxyapatite. J. Surf. Investig. № 5. Р. 863.).

  7. Юрова К.А., Хазиахматова О.Г., Малащенко В.В., Норкин И.К., Иванов П.А., Хлусов И.А., Шунькин Е.О., Тодосенко Н.М., Мелащенко Е.С., Литвинова Л.С. 2020. Клеточно-молекулярные аспекты воспаления, ангиогенеза и остеогенеза. Краткий обзор. Цитология. Т. 62. № 5. С. 305. (Yurova K.A., Khaziakhmatova O.G., Malashchenko V.V., Norkin I.K., Ivanov P.A., Khlusov I.A., Shunkin E.O., Todosenko N.M., Melashchenko E.S., Litvinova L.S. 2020. Cellular and molecular aspects of inflammation, angiogenesis and osteogenesis. Short review. Tsitologiya. V. 62. № 5. Р. 305.).

  8. Albee F.H. 1920. Studies in bone growth: triple calcium phosphate as a stimulus to osteogenesis. Ann. Surg. V. 71. P. 32.

  9. Anderson J.M., Rodriguez A., Chang D.T. 2008. Foreign body reaction to biomaterials. Seminars Immunol. V. 20. P. 86.

  10. Barradas A.M., Fernandes H.A., Groen N., Chai Y.C., Schrooten J., van de Peppel J., van Leeuwen J.V., van Blitterswijk C.V., de Boer J. 2012. A calcium-induced signaling cascade leading to osteogenic differentiation of human bone marrow-derived mesenchymal stromal cells. Biomaterials. V. 33. P. 3205.

  11. Barradas A.M., Yuan H., van Blitterswijk C.A.C., Habibovic P. 2011. Osteoinductive biomaterials: current knowledge of properties, experimental models and biological mechanisms. Eur. Cells Mater. V. 21. P. 407.

  12. Batoon L., Millard S.M., Raggatt L.J., Pettit A.R. 2017a. Osteomacs and bone regeneration. Curr. Osteoporos Rep. V. 15. P. 385.

  13. Batoon L., Millard S.M., Wullschleger M.E., Preda C., Wu A.C.-K, Kaur S., Tseng H.-W., Hume D.A., Levesque J.-P., Raggatt L.J., Pettit A.R. 2017b. CD169 + macrophages are critical for osteoblast maintenance and promote intramembranous and endochondral ossification during bone repair. Biomaterials. V. 196. P. 51.

  14. Bellows C.G., Aubin J.E., Heersche J.N. 1991.Initiation and progression of mineralization of bone nodules formed in vitro: the role of alkaline phosphatase and organic phosphate. Bone Min. V. 14. P. 27.

  15. Ben-Nissan B. 2014. Advances in calcium phosphate biomaterials. Springer Berlin: Heidelberg. P. 547.

  16. Berube P., Yang Y., Carnes D.L., Stover R.E., Boland E.J., Ong J.L. 2005. The effect of sputtered calcium phosphate coatings of different crystallinity on osteoblast differentiation. J. Periodontol. V. 76. P. 1697.

  17. Bianchi M., Urquia Edreira E.R., Wolke J.G., Birgani Z.T., Habibovic P., Jansen J.A., Tampieri A., Marcacci M., Leeuwenburgh S.C., van den Beucken J.J. 2014. Substrate geometry directs the in vitro mineralization of calcium phosphate ceramics. Acta Biomater. V. 10. P. 661.

  18. Bohner M., Miron R.J. 2018. A proposed mechanism for material-induced heterotopic ossification, Mater. Today. V. 22. P. 132.

  19. Boix T., Gomez-Morales J., Torrent-Burgues J., Monfort A., Pulgdomenech P., Rodriguez-Clemente R. 2005. Adsorption of recombinant human bone morphogenetic protein rhBMP-2m onto hydroxyapatite. J. Inorg. Biochem. V. 9. P. 1043.

  20. Bulnheim U., Müller P., Neumann H.-G., Peters K., Unger R.E., Kirkpatrick C.J., Rychly J. 2012. Endothelial cells stimulate osteogenic differentiation of mesenchymal stem cells on calcium phosphate scaffolds. J. Tissue Engineering and Regener. Med. V. 8. P. 831.

  21. Campana V., Milano G., Pagano E., Barba M., Cicione C., Salonna G., Lattanzi W., Logroscino G. 2014. Bone substitutes in orthopaedic surgery: from basic science to clinical practice. J. Mater. Sci. Mater Med. V. 25. P. 2445.

  22. Chai Y.C., Roberts S.J., Schrooten J., Luyten F.P. 2011. Probing the osteoinductive effect of calcium phosphate by using an in vitro biomimetic model. Tiss. Eng. A. V. 17. P. 1083.

  23. Chang D.T., Jones J.A., Meyerson H., Colton E., Kwon I.K., Matsuda T., Anderson J.M. 2008. Lymphocyte/macrophage interactions: biomaterial surface-dependent cytokine, chemokine, and matrix protein production. J. Biomed. Mater. Res. A. V. 87. P. 676.

  24. Chen L., Mccrate J.M., Lee J.C., Li H. 2011. The role of surface charge on the uptake and biocompatibility of hydroxyapatite nanoparticles with osteoblast cells. Nanotechnol. V. 22: 105708.

  25. Chen Z., Wu C., Gu W., Klein T., Crawford R., Xiao Y. 2014. Osteogenic differentiation of bone marrow MSCs by beta-tricalcium phosphate stimulating macrophages via BMP2 signalling pathway. Biomaterials. V. 35. P. 1507.

  26. Combes C., Ray C. 2002. Adsorption of proteins and calcium phosphate materials bioactivity. Biomaterials. V. 23. P. 2817.

  27. Coughlan T., Dockery F. 2014. Osteoporosis and fracture risk in older people. Clin. Med. (Lond). V. 14. P. 187.

  28. Curtis A., Wilkinson C. 1997. Topographical control of cells. Biomaterials. V. 18. P. 1573.

  29. Daculsi G., Legeros R.Z., Nery E., Lynch K., Kerebel B. 1989. Transformation of biphasic calcium phosphate ceramics in vivo: ultrastructural and physicochemical characterization. J. Biomed. Mater. Res. V. 23. P. 883.

  30. Danciu T.E., Adam R.M., Naruse K., Freeman M.R., Hauschka P.V. 2003. Calcium regulates the PI3K-Akt pathway in stretched osteoblasts. FEBS Lett. V. 536. P. 193.

  31. Davies L.C., Rosas M., Jenkins S.J., Liao C.T., Scurr M.J., Brombacher F., Fraser D.J., Allen J.E., Jones S.A., Taylor Ph.R. 2013. Distinct bone marrow-derived and tissue-resident macrophage lineages proliferate at key stages during inflammation. Nat. Commun. V. 4. P. 1886.

  32. Davison N.L., Gamblin A.L., Layrolle P., Yuan H., de Bruijn J.D., Barrere-de Groot F. 2014. Liposomal clodronate inhibition of osteoclastogenesis and osteoinduction by submicrostructured beta-tricalcium phosphate. Biomaterials. V. 35. P. 5088.

  33. Diaz-Flores L., Gutierrez R., Lopez-Alonso A., Gonzalez R., Varela H. 1992. Pericytes as a supplementary source of osteoblasts in periosteal osteogenesis. Clin. Orthop. Relat. Res. V. 275. P. 280.

  34. Dimitriou R., Tsiridis E., Giannoudis P.V. 2005. Current concepts of molecular aspects of bone healing. Injury. V. 36. P. 1392.

  35. Du C., Cui F.Z., Zhang W., Feng Q.L., Zhu X.D., de Groot K. 2000. Formation of calcium phosphate/collagen composites through mineralization of collagen matrix. J. Biomed. Mater. Res. V. 50. P. 518.

  36. Ebrahimi M. 2021. Porosity parameters in biomaterial science: Definition, impact, and challenges in tissue engineering. Front. Mater. Sci. V. 15. P. 352.

  37. Edwards F.C., Taheri A., Dann S.C., Dye J.F. 2011. Characterization of cytolytic neutrophil activation in vitro by amorphous hydrated calcium phosphate as a model of biomaterial inflammation. J. Biomed. Mater. Res. A. V. 96. P. 552.

  38. Ekegren C.L., Edwards E.R., de Steiger R., Gabbe B.J. 2018. Incidence, costs and predictors of non-union, delayed union and mal-union following long bone fracture. Int. J. Environ. Res. Public Health. V. 15. P. 2845.

  39. El-Rashidy A.A., Roether J.A., Harhaus L., Kneser U., Boccaccini A.R. 2017. Regenerating bone with bioactive glass scaffolds: a review of in vivo studies in bone defect models. Acta Biomater. V. 62. P. 1.

  40. Fellah B.H., Gauthier O., Weiss P., Chappard D., Layrolle P. 2008. Osteogenicity of biphasic calcium phosphate ceramics and bone autograft in a goat model. Biomaterials. V. 29. P. 1177.

  41. Feng B., Weng J., Yang B.C., Qu S.X., Zhang X.D. 2004. Characterization of titanium surfaces with calcium and phosphate and osteoblast adhesion. Biomaterials. V. 25. P. 3421.

  42. Feng W. 2014. Osteoclastogenesis and osteoimmunology. Front. Biosci. V. 19. P. 758.

  43. Fillingham Y., Jacobs J. 2014. Bone grafts and their substitutes. J. Indian Soc. Periodontol. V. 18. P. 610.

  44. Flade K., Lau C., Mertig M., Pompe W. 2001. Osteocalcin-controlled dissolution-reprecipitation of calcium phosphate under biometric conditions. Chem. Mater. V. 13. P. 3596.

  45. Foreman M.A., Gu A.Y., Howl J.D., Jones S., Publicover S.J. 2005. Group III metabotropic glutamate receptor activation inhibits Ca2+ influx and nitric oxide synthase activity in bone marrow stromal cells. J. Cell Physiol. V. 204. P. 704.

  46. Gamblin A.-L., Brennan M.A., Renaud A., Yagita H., Lézot F., Heymann D., Trichet V., Layrolle P. 2014. Bone tissue formation with human mesenchymal stem cells and biphasic calcium phosphate ceramics: the local implication of osteoclasts and macrophages. Biomaterials. V. 35. P. 9660.

  47. Garg P., Mazur M.M., Buck A.C., Wandtke M.E., Liu J., Ebraheim N.A. 2017. Prospective review of mesenchymal stem cells differentiation into osteoblasts. Orthop Surg. V. 9. P. 13.

  48. Ghosh S.K., Nandi S.K., Kundu B., Datta S., De D.K., Roy S.K., Basu D. 2008. In vivo response of porous hydroxyapatite and beta-tricalcium phosphate prepared by aqueous solution combustion method and comparison with bioglass scaffolds. J. Biomed. Mater. Res. B. Appl. Biomater. V. 86. P. 217.

  49. Goding J.W., Grobben B., Slegers H. 2003. Physiological and pathophysiological functions of the ecto-nucleotide pyrophosphatase/phosphodiesterase family. Biochim. Biophys. Acta Mol. Basis Dis. V. 1638. P. 1.

  50. Gustavsson J., Ginebra M. P., Planell J., Engel E. 2012. Osteoblast-like cellular response to dynamic changes in the ionic extracellular environment produced by calcium-deficient hydroxyapatite. JMSMM. V. 23. P. 2509.

  51. Habibovic P., Sees T.M., van den Doel M.A., van Blitterswijk C.A., de Groot J.K. 2006. Osteoinduction by biomaterials–physicochemical and structural influences. Biomed. Mater. Res. A. V. 77. P. 747.

  52. Hasegawa T., Hongo H., Yamamoto T., Abe M., Yoshino H., Haraguchi-Kitakamae M., Ishizu H., Shimizu T., Iwasaki N., Amizuka N. 2022. Matrix vesicle-mediated mineralization and osteocytic regulation of bone mineralization. Int. J. Mol. Sci. V. 23. P. 9941.

  53. Henriksen K., Karsdal M.A., John Martin T. 2014. Osteoclast-derived coupling factors in bone remodeling. Calcif. Tiss. Int. V. 94 P. 88.

  54. Hu Q.H., Tan Z., Liu Y.K., Tao J.H., Cai Y.R., Zhang M., Pan H., Xu X., Tang R. 2007. Effect of crystallinity of calcium phosphate nanoparticles on adhesion, proliferation, and differentiation of bone marrow mesenchymal stem cells. J. Mater. Chem. V. 17. P. 4690.

  55. Humbert P., Brennan M.Á., Davison N., Rosset Ph., Trichet V., Blanchard F., Layrolle P. 2019. immune modulation by transplanted calcium phosphate biomaterials and human mesenchymal stromal cells in bone regeneration. Front. Immunol. V. 10. P. 663.

  56. Ikebuchi Y., Aoki S., Honma M., Hayashi M., Sugamori Y., Khan M., Kariya Y., Kato G., Tabata Y., Penninger J.M., Udagawa N., Aoki K., Suzuki H. 2018. Coupling of bone resorption and formation by RANKL reverse signalling. Nature. V. 561. P. 195.

  57. James A.W. 2013. Review of signaling pathways governing MSC osteogenic and Adipogenic differentiation. Scientifica (Cairo). 2013: 684736.

  58. Jensen S.S., Bosshardt D.D., Gruber R., Buser D. 2014. Long-term stability of contour augmentation in the esthetic zone: histologic and histomorphometric evaluation of 12 human biopsies 14 to 80 months after augmentation. J. Periodontol. V. 85. P. 1549.

  59. Jeong J., Kim J.H., Shim J.H., Hwang N.S., Heo C.Y. 2019. Bioactive calcium phosphate materials and applications in bone regeneration. Biomater. Res. V. 23. P. 4.

  60. John A., Varma H.K., Kumari T.V. 2003. Surface reactivity of calcium phosphate based ceramics in a cell culture system. J. Biomater. V. 18. P. 63.

  61. Julien M., Khoshniat S., Lacreusette A., Gatius M., Bozec A., Wagner E.F., Wittrant Y., Masson M., Weiss P., Beck L., Magne D., Guicheux J. 2009. Phosphate-dependent regulation of MGP in osteoblasts: role of ERK1/2 and Fra-1. J. Bone Miner. Res. V. 24. P. 1856.

  62. Jung G.Y., Park Y.J., Han J.S. 2010. Effects of HA released calcium ion on osteoblast differentiation. J. Mater. Sci. Mater. Med. V. 21. P. 1649.

  63. Kandori K., Miyagawa K., Ishikawa T. 2004. Adsorption of immunogamma globulin onto various synthetic calcium hydroxyapatite particles. J. Colloid. Interface Sci. V. 273. P. 406.

  64. Kandori K., Murata K., Ishikawa T. 2007. Microcalorimetric study of protein adsorption onto calcium hydroxyapatites. Langmuir. V. 23. P. 2064.

  65. Karalashvili L., Kakabadze A., Uhryn M., Vyshnevska H., Ediberidze K., Kakabadze Z. 2018. Bone grafts for reconstruction of bone defects (review). Georgian Med. News. V. 282. P. 44.

  66. Katsuyama E., Miyamoto H., Kobayashi T., Sato Y., Hao W., Kanagawa H., Fujie A., Tando T., Watanabe R., Morita M., Miyamoto K., Niki Y., Morioka H., Matsumoto M., Toyama Y. et al. 2015. Interleukin-1 receptor-associated kinase-4 (IRAK4) promotes inflammatory osteolysis by activating osteoclasts and inhibiting formation of foreign body giant cells. J. Biol. Chem. V. 290. P. 716.

  67. Khlusov I.A., Khlusova M.Yu., Zaitsev K.V., Kolokol’tsova T.D., Sharkeev Yu.P., Pichugin V.F., Legostaeva E.V., Trofi mova I.E., Klimov A.S., Zhdanova A.I. 2011. Pilot in vitro study of the parameters of artificial niche for osteogenic differentiation of human stromal stem cell pool. Bull. Exp. Biol. Med. V. 150. P. 535.

  68. Khlusov I.A., Litvinova L.S., Shupletsova V.V., Khaziakhmatova O.G., Malashchenko V.V., Yurova K.A., Shunkin E.O., Krivosheev V.V., Porokhova E.D., Sizikova A.E., Safiullina L.A., Legostaeva E.V., Komarova E.G., Sharkeev Yu.P. 2020. Costimulatory effect of rough calcium phosphate coating and blood mononuclear cells on adipose-derived mesenchymal stem cells in vitro as a model of in vivo tissue repair. Materials. V. 13. P. 4398.

  69. Khlusov I.A., Litvinova L.S., Yurova K.A., Khlusova M.Y. 2022. Precise tissue bioengineering and niches of mesenchymal stem cells: their size and hierarchy matter. Biocell. V. 46. P. 1635.

  70. Khlusov I.A., Shevtsova N.M., Khlusova M.Y. 2013. Detection in vitro and quantitative estimation of artificial microterritories which promote osteogenic differentiation and maturation of stromal stem cells. Methods Mol. Biol. V. 1035. P. 103.

  71. Khlusov I.A., Dekhtyar Y., Sharkeev Y.P., Pichugin V.F., Khlusova M.Y., Polyaka N., Tjulkins F., Vendinya V., Legostaeva E.V., Litvinova L.S., Shupletsova V.V., Khaziakhmatova O.G., Yurova K.A., Prosolov K.A. 2018. Nanoscale electrical potential and roughness of a calcium phosphate surface promotes the osteogenic phenotype of stromal cells. Materials. V. 11. P. 978.

  72. Khoshniat S., Bourgine A., Julien M., Petit M., Pilet P., Rouillon T., Masson M., Gatius M., Weiss P., Guicheux J., Beck L. 2011. Phosphatedependent stimulation of MGP and OPN expression in osteoblasts via the ERK1/2 pathway is modulated by calcium. Bone. V. 48. P. 894.

  73. Kim S.E., Park K. 2020. Recent advances of biphasic calcium phosphate bioceramics for bone tissue regeneration. Adv. Exp. Med. Biol. V. 1250. P. 177.

  74. Knabe C., Driessens F.C.M., Planell J. A., Gildenhaar R., Berger G., Reif D., Fitzner R., Radlanski R.J., Gross U. 2000. Evaluation of calcium phosphates and experimental calcium phosphate bone cements using osteogenic cultures. J. Biomed. Mater. Res. V. 52. P. 498.

  75. Komarova E.G., Sharkeev Y.P., Sedelnikova M.B., Prymak O., Epple M., Litvinova L.S., Shupletsova V.V, Malashchenko V.V., Yurova K.A., Dzyuman A.N., Kulagina I.V., Mushtovatova L.S., Bochkareva O.P., Karpova M.R., Khlusov I.A. 2020. Zn- or Cu-containing CaP-based coatings formed by micro-arc oxidation on titanium and Ti-40Nb alloy: part II – wettability and biological performance. Materials. V. 13. P. 4366.

  76. Kuroda Y., Hisatsune Ch., Nakamura T., Matsuo K., Mikoshiba K. 2008. Osteoblasts induce Ca2+ oscillation-independent NFATc1 activation during osteoclastogenesis. Proc. Natl. Acad Sci. USA. V. 105. P. 8643.

  77. Li B., Liao X.L., Zheng L., Zhu X. D., Wang Z., Fan H.S., Zhang X. 2012. Effect of nanostructure on osteoinduction of porous biphasic calcium phosphate ceramics. Acta Biomater. V. 8. P. 3794.

  78. Litvinova L., Yurova K., Shupletsova V., Khaziakhmatova O., Malashchenko V., Shunkin E., Melashchenko E., Todosenko N., Khlusova M., Sharkeev Y., Komarova E., Sedelnikova M., Khlusov I. 2020. Gene expression regulation and secretory activity of mesenchymal stem cells upon in vitro contact with microarc calcium phosphate coating. Int. J. Mol. Sci. V. 21. P. 7682.

  79. Liu D., Genetos D.C., Shao Y., Geist D.J., Li J., Ke H.Zh., Turner Ch.H., Duncan R.L. 2008. Activation of extracellular-signal regulated kinase (ERK1/2) by fluid shear is Ca2+ and ATP-dependent in MC3T3-E1 osteoblasts. Bone. V. 42. P. 644.

  80. Liu Q., Lu W.F., Zhai W. 2022. Toward stronger robocast calcium phosphate scaffolds for bone tissue engineering: A mini-review and meta-analysis. Biomater. Adv. V. 134. P. 112 578.

  81. Liu Y.K., Lu Q.Z., Pei R., Ji H.J., Zhou G.S., Zhao X.L., Tang R.K., Zhang M. 2009. The effect of extracellular calcium and inorganic phosphate on the growth and osteogenic differentiation of mesenchymal stem cells in vitro: implication for bone tissue engineering. Biomed. Mater. V. 4: 025004.

  82. MacLauchlan S., Skokos E.A., Meznarich N., Zhu D.H., Raoof S., Shipley J.M., Senior R.M., Bornstein P., Kyriakides Th.R. 2009. Macrophage fusion, giant cell formation, and the foreign body response require matrix metalloproteinase 9. J. Leukoc. Biol. V. 85. P. 617.

  83. Mafina M.K., Sullivan A.C., Hing K.A. 2017. Use of a fluorescent probe to monitor the enhanced affinity of rh-BMP-2 to silicated-calcium phosphate synthetic bone graft substitutes under competitive conditions. Mater. Sci. Eng. C Mater. Biol. Appl. V. 80. P. 207.

  84. Maggiano I.S., Maggiano C.M., Clement J.G., Thomas C.D., Carter Y., Cooper D.M. 2016. Three-dimensional reconstruction of Haversian systems in human cortical bone using synchrotron radiation-based micro-CT: morphology and quantification of branching and transverse connections across age. J. Anat. May. V. 228. P. 719.

  85. Majidinia M., Sadeghpour A., Yousefi B. 2018. The roles of signaling pathways in bone repair and regeneration. J. Cell Physiol. V. 233. P. 2937.

  86. Maloney M.A., Dorie M.J., Lamela R.A., Rogers Z.R., Patt H.M. 1978. Hematopoietic stem cell regulatory volumes as revealed in studies of the bgj/bgj:W/WV chimera. J. Exp. Med. V. 147. P. 1189.

  87. Mao L., Liu J., Zhao J., Chang J., Xia L., Jiang L., Wang X., Lin K., Fang B. 2015. Effect of micro-nano-hybrid structured hydroxyapatite bioceramics on osteogenic and cementogenic differentiation of human periodontal ligament stem cell via Wnt signaling pathway. Int. J. Nanomedicine. V. 8. P. 1887.

  88. Marino G., Rosso F., Cafiero G., Tortora C., Moraci M., Barbarisi M., Barbarisi A. 2010. Beta-tricalcium phosphate 3D scaffold promote alone osteogenic differentiation of human adipose stem cells: in vitro study. J. Mater. Sci. Mater. Med. V. 21. P. 353.

  89. Matsuura T., Hosokawa R., Okamoto K., Kimoto T., Akagawa Y. 2000. Diverse mechanisms of osteoblast spreading on hydroxyapatite and titanium. Biomaterials. V. 21. P. 1121.

  90. McNally A.K., Anderson J.M. 1995. Interleukin-4 induces foreign body giant cells from human monocytes/macrophages. Differential lymphokine regulation of macrophage fusion leads to morphological variants of multinucleated giant cells. Am. J. Pathol. V. 147. P. 1487.

  91. McNally A.K., Anderson J.M. 2011. Foreign body-type multinucleated giant cells induced by interleukin-4 express select lymphocyte co-stimulatory molecules and are phenotypically distinct from osteoclasts and dendritic cells. Exp. Mol. Pathol. V. 91. P. 673.

  92. McNally A.K., Jones J.A., MacEwan S.R., Colton E., Anderson J.M. 2008. Vitronectin is a critical protein adhesion substrate for IL-4-induced foreign body giant cell formation. J. Biomed. Mater. Res. A. V. 86A. P. 35.

  93. McNally A.K., Macewan S.R., Anderson J.M. 2007. Alpha subunit partners to beta1 and beta2 integrins during IL-4-induced foreign body giant cell formation. J. Biomed. Mater. Res. Part A. V. 82. P. 568.

  94. Meleti Z., Shapiro M., Adams C.S. 2000. Inorganic phosphate induces apoptosis of osteoblast-like cells in culture. Bone. V. 27. P. 359.

  95. Millan C., Vivanco J.F., Benjumeda-Wijnhoven I.M., Bjelica S., Santibanez J.F. 2018. Mesenchymal stem cells and calcium phosphate bioceramics: implications in periodontal bone regeneration. Adv. Exp. Med. Biol. V. 1107. P. 91.

  96. Miron R.J., Bosshardt D.D. 2016. OsteoMacs: key players around bone biomaterials. Biomaterials. V. 82. P. 1.

  97. Moreno J.L., Mikhailenko I., Tondravi M.M., Keegan A.D. 2007. IL-4 promotes the formation of multinucleated giant cells from macrophage precursors by a STAT6-dependent, homotypic mechanism: contribution of E-cadherin. J. Leukoc. Biol. V. 82. P. 1542.

  98. Murshed M. 2018. Mechanism of bone mineralization. Cold Spring Harb. Perspect. Med. V. 8: a031229. Erratum in: Cold Spring Harb. Perspect. Med. 2020. V. 10.

  99. Najar M., Raicevic G., Crompot E., Fayyad-Kazan H., Bron D., Toungouz M., Lagneaux L. 2016. The immunomodulatory potential of mesenchymal stromal cells. J. Immunother. V. 39. P. 45.

  100. Nich C., Takakubo Y., Pajarinen J., Ainola M., Salem A., Sillat T., Rao A.J., Raska M., Tamaki Y., Takagi M., Konttinen Y.T., Goodman St.B., Gallo J. 2013. Macrophages-key cells in the response to wear debris from joint replacements. J. Biomed. Mater. Res. A. V. 101. P. 3033.

  101. Nudelman F., Pieterse K., George A., Bomans P.H.H., Friedrich H., Brylka L.J., Hilbers P.A.J., de With G., Sommerdijk N.A.J.M. 2010. The role of collagen in bone apatite formation in the presence of hydroxyapatite nucleation inhibitors. Nat. Mater. V. 9. P. 1004.

  102. Ogata K., Katagiri W., Hibi H. 2017. Secretomes from mesenchymal stem cells participate in the regulation of osteoclastogenesis in vitro. Clin. Oral Investig. V. 21. P. 1979.

  103. Okamoto K., Takayanagi H. 2019. Osteoimmunology. Cold Spring Harb. Perspect. Med. V. 9: a031245.

  104. Orimo H. 2010. The mechanism of mineralization and the role of alkaline phosphatase in health and disease. J. Nippon Med. Sch. V. 77. P. 4.

  105. Othman Z., Fernandes H., Groot Arjan J, Luider Theo M., Alcinesio A., de Melo Pereira D., Guttenplan Al.P.M., Yuan H., Habibovic P. 2019. The role of ENPP1/PC-1 in osteoinduction by calcium phosphate ceramics Biomaterials. V. 210. P. 12.

  106. Pajarinen J., Lin T., Gibon E., Kohno Y., Maruyama M., Nathan K., Lu L., Yao Zh., Goodman St.B. 2018. Mesenchymal stem cell-macrophage crosstalk and bone healing. Biomaterials. V. 196. P. 80.

  107. Pchelintseva E., Djamgoz M.B.A. 2018. Mesenchymal stem cell differentiation: Control by calcium-activated potassium channels. J. Cell Physiol. V. 233. P. 3755.

  108. Polini A., Pisignano D., Parodi M., Quarto R., Scaglione S. 2011. Osteoinduction of human mesenchymal stem cells by bioactive composite scaffolds without supplemental osteogenic growth factors. PLoS One. V. 6: e26211.

  109. Quinn JM.W., Itoh K., Udagawa N., Häusler K., Yasuda H., Shima N., Mizuno A., Higashio K., Takahashi N., Suda T., Martin T.J., Gillespie M.T. 2001. Transforming growth factor β affects osteoclast differentiation via direct and indirect actions. J. Bone Miner. Res. V. 16. P. 1787.

  110. Rana N., Suliman S., Mohamed-Ahmed S., Gavasso S., Gjertsen B.T., Mustafa K. 2022. Systemic and local innate immune responses to surgical co-transplantation of mesenchymal stromal cells and biphasic calcium phosphate for bone regeneration. Acta Biomater. Actions. V. 141. P. 440.

  111. Raphel J., Holodniy M., Goodman S.B., Heilshorn S.C. 2016. Multifunctional coatings to simultaneously promote osseointegration and prevent infection of orthopaedic implants. Biomaterials. V. 84. P. 301.

  112. Ratner B.D., Hoffman A.S., Schoen F., Lemons J. (Eds.) 2004. Biomaterials science: an introduction to materials in medicine. San Diego, CA, USA: Elsevier Acad. Press. 864 p.

  113. Ripamonti U., Roden L.C. 2010. Induction of bone formation by transforming growth factor-beta2 in the non-human primate Papio ursinus and its modulation by skeletal muscle responding stem cells. Cell Prolif. V. 43. P. 207.

  114. Ripamonti U., Roden L.C., Ferretti C., Klar R.M. 2011. Biomimetic matrices self-initiating the induction of bone formation. J. Craniofac. Surg. V. 22. P. 1859.

  115. Rodriguez A., Macewan S.R., Meyerson H., Kirk J.T., Anderson J.M. 2009. The foreign body reaction in T-cell-deficient mice. J. Biomed. Mater. Res. A. V. 90. P. 106.

  116. Sadowska J.M, Wei F., Guo J., Guillem-Marti J., Lin Zh., Ginebra M.-P., Xiao Y. 2019. The effect of biomimetic calcium deficient hydroxyapatite and sintered β-tricalcium phosphate on osteoimmune reaction and osteogenesis. Acta Biomater. V. 96. P. 605.

  117. Salasznyk R.M., Klees R.F., Williams W.A., Boskey A., Plopper G.E. 2007. Focal adhesion kinase signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells. Exp. Cell Res. V. 313. P. 22.

  118. Samavedi S., Whittington A.R., Goldstein A.S. 2013. Calcium phosphate ceramics in bone tissue engineering: a review of properties and their influence on cell behavior. Acta Biomater. V. 9. P. 8037.

  119. Sapir-Koren R., Livshits G. 2011. Bone mineralization and regulation of phosphate homeostasis. IBMS BoneKEy. V. 8. P. 286.

  120. Schemitsch E.H. 2017. Size matters: defining critical in bone defect size! J. Orthop. Trauma. V. 31. P. S20.

  121. Shen B., Bhargav D., Wei A., Williams L. A., Tao H., Ma D.D.F., Diwan A.D. 2009. BMP-13 emerges as a potential inhibitor of bone formation. Int. J. Biol. Sci. V. 5. P. 192.

  122. Shi F., Fang X., Zhou T., Huang X., Duan K., Wang J., Qu S., Zhi W., Weng J. 2022. Macropore regulation of hydroxyapatite osteoinduction via microfluidic pathway. Int. J. Mol. Sci. V. 23. P. 11459.

  123. Silva L.H.A., Antunes M.A., Dos Santos C.C., Weiss D.J., Cruz F.F., Rocco P.R.M. 2018. Strategies to improve the therapeutic effects of mesenchymal stromal cells in respiratory diseases. Stem Cell Res. Ther. V. 9. P. 45.

  124. Sims N.A., Martin T.J. 2014. Coupling the activities of bone formation and resorption: a multitude of signals within the basic multicellular unit. Bonekey Rep. V. 3. P. 1.

  125. Sokolova V., Knuschke T., Kovtun A., Buer J., Epple M., Westendorf A.M. 2010. The use of calcium phosphate nanoparticles encapsulating Toll-like receptor ligands and the antigen hemagglutinin to induce dendritic cell maturation and T cell activation. Biomaterials. V. 31. P. 5627.

  126. Stephansson S.N., Byers B.A., Garcia A.J. 2002. Enhanced expression of the osteoblastic phenotype on substrates that modulate fibronectin conformation and integrin receptor binding. Biomaterials. V. 23. P. 2527.

  127. Tada H., Nemoto E., Foster B.L., Somerman M.J., Shimauchi H. 2011. Phosphate increases bone morphogenetic protein-2 expression through cAMP-dependent protein kinase and ERK1/2 pathways in human dental pulp cells. Bone. V. 48. P. 1409.

  128. Takeshita S., Fumoto T., Matsuoka K., Park K., Aburatani H., Kato S., Ito M., Ikeda K. 2013. Osteoclast-secreted CTHRC1 in the coupling of bone resorption to formation. J. Clin. Invest. V. 123. P. 3914.

  129. Teitelbaum S.L. 2005. Osteoporosis and integrins, J. Clin. Endocrinol. Metab. V. 90. P. 2466.

  130. Ten Harkel B., Schoenmaker T., Picavet D.I., Davison N.L., de Vries T.J., Everts V. 2015. The foreign body giant cell cannot resorb bone, but dissolves hydroxyapatite like osteoclasts. PLoS ONE. V. 10: e0139564.

  131. Thrivikraman G., Athirasala A., Twohig C., Boda S.K., Bertassoni L.E. 2017. Biomaterials for craniofacial bone regeneration. Dent Clin. North Am. V. 61. P. 835.

  132. Tsapikouni T.S., Missirlis Y.F. 2008. Protein–material interactions: from micro-to-nano scale. Mater. Sci. Eng. B. V. 152. P. 2.

  133. van Furth R., Cohn Z.A. 1968. The origin and kinetics of mononuclear phagocytes. J. Exper. Med. V. 128. P. 415.

  134. Vasconcelos D.P., Costa M., Amaral I.F., Barbosa M.A., Aguas A.P., Barbosa J.N. 2015. Modulation of the inflammatory response to chitosan through M2 macrophage polarization using pro-resolution mediators. Biomaterials. V. 37. P. 116.

  135. Viti F., Landini M., Mezzelani A., Petecchia L., Milanesi L., Scaglione S. 2016. Osteogenic differentiation of MSC through calcium signaling activation: transcriptomics and functional analysis. PLoS One. V. 11: e0148173.

  136. Vulf M., Khlusov I., Yurova K., Todosenko N., Komar A., Kozlov I., Malashchenko V., Shunkina D., Khaziakhmatova O., Litvinova L. 2022. MicroRNA regulation of bone marrow mesenchymal stem cells in the development of osteoporosis in obesity. Front. Biosci. (Schol Ed). V. 14. P. 17.

  137. Wang Y., Hu J., Jiao J., Liu Z., Zhou Z., Zhao C., Chang L.J., Chen Y.E., Ma P.X., Yang B. 2014. Engineering vascular tissue with functional smooth muscle cells derived from human iPS cells and nanofibrous scaffolds. Biomaterials. V. 35. P. 8960.

  138. Xiao D., Zhang J., Zhang C., Barbieri D., Yuan H., Moroni L., Feng G. 2020. The role of calcium phosphate surface structure in osteogenesis and the mechanisms involved. Acta Biomater. V. 106. P. 22.

  139. Yuan H.P., Fernandes H., Habibovic P., de Boer J., Barradas AM.C., de Ruiter A., Walsh W.R., van Blitterswijk C.A., de Bruijn J.D. 2010. Osteoinductive ceramics as a synthetic alternative to autologous bone grafting. Proc. Natl. Acad. Sci. USA. V. 107. P. 13614.

  140. Yurova K.A., Melashchenko E.S., Khaziakhmatova O.G., Malashchenko V.V., Melashchenko O.B., Shunkin E.O., Norkin I.K., Ivanov P.A., Khlusov I.A., Litvinova L.S. 2021. Osteogenic differentiation factors of multipotent mesenchymal stromal cells in the current understanding. Curr. Pharm. Des. V. 27. P. 3741.

  141. Zayzafoon M., Fulzele K., McDonald J.M. 2005. Calmodulin and calmodulin-dependent kinase IIalpha regulate osteoblast differentiation by controlling c-fos expression. J. Biol. Chem. V. 280. P. 7049.

  142. Zhang R., Lu Y., Ye L., Yuan B., Yu Sh., Qin Ch., Xie Y., Gao T., Drezner M.K., Bonewald L.F., Feng J.Q. 2011. Unique roles of phosphorus in endochondral bone formation and osteocyte maturation. J. Bone Miner. Res. V. 26. P. 1047.

  143. Zhang Y., Böse T., Unger R.E., Jansen J.A., Kirkpatrick C.J., van den Beucken J.P. 2017. Macrophage type modulates osteogenic differentiation of adipose tissue MSCs. Cell Tiss. Res. V. 369. P. 273.

  144. Zhao L., Kaye A.D., Kaye A.J., Abd-Elsayed A. 2018. Stem cell therapy for osteonecrosis of the femoral head: current trends and comprehensive review. Curr. Pain Headache Rep. V. 22. P. 41.

  145. Zhao Z., Zhao Q., Gu B., Yin C., Shen K., Tang H., Xia H., Zhang X., Zhao Y., Yang X., Zhang Y. 2020. Minimally invasive implantation and decreased inflammation reduce osteoinduction of biomaterial. Theranostics. V. 10. P. 3533.

  146. Zhu X.D., Fan H.S., Li D.X., Xiao Y.M., Zhang X.D. 2007. Protein adsorption and zeta potentials of a biphasic calcium phosphate ceramic under various conditions. J. Biomed. Mater. Res B. V. 82B. P. 65.

  147. Zhu X.D., Fan H.S., Xiao Y.M., Li D.X., Zhang H.J., Luxbacher T., Zhang X.D. 2009. Effect of surface structure on protein adsorption to biphasic calcium-phosphate ceramics in vitro and in vivo. Acta Biomater. V. 5. P. 1311.

  148. Zhu X., Zhang H.J., Fan H.S., Li W., Zhang X.D. 2010. Effect of phase composition and microstructure of calcium phosphate ceramic particles on protein adsorption. Acta Biomater. V. 6. P. 1536.

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