POSSIBILITIES OF CURRENT CELLULAR TECHNOLOGIES FOR ARTICULAR CARTILAGE REPAIR (ANALYTICAL REVIEW)

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Abstract

Despite a wide variety of surgical procedures utilized in clinical practice for treatment of articular cartilage lesions, the search for other options of articular reconstruction remains a relevant and open issue at the current stage of medicine and biotechnologies development. The recent years demonstrated a strong belief in cellular methods of hyaline cartilage repair such as implantation of autologous chondrocytes (ACI) or cultures of mesenchymal stem cells (MSC) including techniques for genetic modification of cells.

The purpose of presented review is to summarize the published scientific data on up to date results of perspective cellular technologies for articular cartilage repair that are being developed. Autologous chondrocyte transplantation originally performed by Swedish researchers in 1987 is considered the first clinically applied technique for restoration of hyaline cartilage using cellular technologies. However, the transplanted cell culture featured low proliferative capacity and inability to form a regenerate resistant to high physical activity. Another generation of methods originated at the turn of the century utilized mesenchymal stem cells instead of autologous chondrocytes. Preparation of MSCs is a less invasive procedure compared to chondrocytes harvesting and the culture is featured by a higher proliferative ability. Researchers use various biodegradable carriers (matrices) to secure cell fixation. Despite good clinical mid-term outcomes the transplanted tissue-engineering structures deteriorate with time due to cellular de-differentiation. Next generation of techniques being currently under pre-clinical studies is featured by the preliminary chondrogenic modification of transplanted cell culture. Usage of various growth factors, modified cell product and gene-activated matrices allow to gain a stable regulatory and key proteins synthesis and achieve a focused influence on regenerate's chondrogenic proliferation and in result to form a good hyaline cartilage resistant to high physical load in long term period.

Thus, development of methods for articular cartilage repair has long ago went beyond the interests of clinical physicians, and only the close interdisciplinary cooperation of clinicians and specialists for cytology, molecular genetics and, probably, virology would enable replacement of a defect with a rigorous hyaline cartilage.

About the authors

M. S. Bozhokin

Vreden Russian Research Institute of Traumatology and Orthopedics, St. Petersburg

Author for correspondence.
Email: writeback@mail.ru

Bozhokin Mikhail S. - assistant researcher.

Ul. Akad. Baykova, 8, St. Petersburg, Russia, 195427, e-mail: writeback@mail.ru

Russian Federation

S. A. Bozhkova

Vreden Russian Research Institute of Traumatology and Orthopedics, St. Petersburg

Email: fake@neicon.ru

Bozhkova Svetlana A. - head of the research Department of prevention and treatment of wound infection and Department of clinical pharmacology

Russian Federation

G. I. Netylko

Vreden Russian Research Institute of Traumatology and Orthopedics, St. Petersburg

Email: fake@neicon.ru

Netylko Georgy I. - head of the research Department of experimental morphology

Russian Federation

References

  1. Божкова С.А., Буянов А.Л., Кочиш А.Ю., Румакин В.п., Хрипунов А.К., Нетылько Г.И., Смыслов Р.Ю., Афанасьев А.В., панарин Е.ф. перифокальные тканевые реакции на имплантацию образцов гидрогелевого материала на основе полиа-криламида с добавлением целлюлозы (экспериментальное исследование). Морфология. 2016;149(2):47-53.
  2. Брянская А.И., Куляба Т.А., Корнилов Н.Н., Румакин В.п., Горностаев В.С. Артропластика с использованием аутологичных мультипотентных ме-зенхимальных клеток и коллагеновой мембраны ChondroGyde®. Вестник травматологии и ортопедии имени Н.Н. Приорова. 2014;1: 62-66.
  3. Деев Р.В., Григорян А.С., Кругляков п.В., Билибина А.А., Соколова И.Б., павличенко Н.Н., полынцев Д.Г. применение трансплантатов, содержащих мультипо-тентные мезенхимальные стромальные клетки, для восстановления поврежденных суставных поверхностей в эксперименте. Гены и клетки. 2010;5(2):44-55.
  4. Нащекина Ю.А., Никонов п.О., Михайлов В.М., пинаев Г. п. зависимость заполнения стромальными клетками костного мозга трёхмерной матрицы от способа посева клеток и типа модификации поверхности матрицы. Цитология. 2014;56(4):283-290.
  5. Новочадов В.В. проблема управления клеточным заселением и ремоделированием тканеинженерных матриц для восстановления суставного хряща (обзор литературы). Вестник Волгоградского государственного университета. Естественные науки. 2013;(1):19-28.
  6. Омельяненко Н.п. Слуцкий Л.И. Соединительная ткань Т.2. М.: Известия; 2009. 378 c.
  7. Советников Н.Н., Кальсин В.А., Коноплянников М.А., Муханов В.В. Клеточные технологии и тканевая инженерия в лечении дефектов суставной поверхности. Клиническая практика. 2013;(1):52-66.
  8. Adesida A.B., Mulet-Sierra a., Jomha N.M. Hypoxia mediated isolation and expansion enhances the chondrogenic capacity of bone marrow mesenchymal stromal cells. Stem Cell Res Ther. 2012;3:9. doi.org/10.1186/scrt100
  9. Bekkers J.E., Tsuchida A.I., van Rijen M.H., Vonk L.A., Dhert W.J., Creemers L.B., Saris D.B. Single-stage cell-based cartilage regeneration using a combination of chondrons and mesenchymal stromal cells: comparison with microfracture. Am J Sports Med. 2013;41(9):2158-2166. doi.org/10.1177/0363546513494181
  10. Brittberg M., Lindahl A., Nilsson A., Ohlsson C., Isaksson O., Peterson L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Eng J Med. 1994; (331): 889-895. doi.org/10.1056/nejm199410063311401
  11. Capeci C.M., Turchiano M., Strauss E.J., Youm T. Osteochondral allografts: applications in treating articular cartilage defects in the knee. Bull Hosp J Dis. 2013;71(1):60-67.
  12. Choi J., Choi В., Park S., Pai K., Li T., Min В., Park S. Mechanical stimulation by ultrasound enhances chondrogenic differentiation of mesenchymal stem cells in a fibrin-hyaluronic acid hydrogel. Artif Organs. 2013; 37(7):648-655. doi: 10.1111/aor.12041.
  13. Darling E., Athanasiou K. Rapid phenotypic changes in passaged articular chondrocyte subpopulations. J Orthop Res. 2005;23(2):425-432. doi.org/10.1016/j.orthres.2004.08.008
  14. Gigante A., Cecconi S., Calcagno S., Busilacchi A., Enea D. Arthroscopic knee cartilage repair with covered microfracture and bone marrow concentrate. Arthrosc Tech. 2012;1:175-180. doi.org/10.1016/j.eats.2012.07.001
  15. Giannini S., Buda R., Vannini F., Cavallo M., Grigolo В. One-step bone marrow-derived cell transplantation in talar osteochondral lesions. Clin Orthop Relat Res. 2009;467:3307-3320. doi.org/10.1007/s11999-009-0885-8
  16. Giannini S., Buda R., Cavallo M., Ruffilli A., Cenacchi A., Cavallo C., Vannini F. Cartilage repair evolution in post-traumatic osteochondral lesions of the talus: from open field autologous chondrocyte to bone-marrow-derived cells transplantation. Injury. 2010;41:1196-1203. doi.org/10.1016/j.injury.2010.09.028
  17. Gille J., Schuseil E., Wimmer J., Gellissen J., Schulz AP., Behrens P. Mid-term results of Autologous Matrix-Induced Chondrogenesis for treatment of focal cartilage defects in the knee. Knee Surg Sports Traumatol Arthrosc. 2010; 18(11):1456-1465. doi.org/10.1007/s00167-010-1042-3
  18. Grigolo В., Lisignoli G., Piacentini A., Fiorini M., Gobbi P., Mazzotti G., Duca M., Pavesio A., Facchini A. Evidence for redifferentiation of human chondrocytes grown on a hyaluronan-based biomaterial (HYAff 11): molecular, immunohistochemical and ultrastructural analysis. Biomaterials. 2002;23(4):1187-1195. doi.org/10.1016/ s0142-9612(01)00236-8
  19. Im G.I. Gene transfer strategies to promote chondrogenesis and cartilage regeneration. Tissue Eng Part B Rev. 2016;22(2):136-148. doi.org/10.1089/ten.teb.2015.0347
  20. Johnstone В., Hering M., Caplan I., Goldberg M., Yoo U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res. 1998;238: 265-272.
  21. Jomha NM, Adesida AB, Bornes TD. Mesenchymal stem cells in the treatment of traumatic articular cartilage defects: a comprehensive review. Arthritis Res Ther. 2014;16:432-451. doi.org/10.1186/s13075-014-0432-1
  22. Karlsen T.A., Shahdadfar A., Brinchmann J.E. Human primary articular chondrocytes, chondroblasts-like cells, and dedifferentiated chondrocytes: differences in gene, microRNA, and protein expression and phenotype. Tissue Eng Part C Methods. 2011;17(2):219-227. doi: 10.1089/ten.TEC.2010.0200
  23. Khan W.S., Tew S.R., Adesida A.B., Hardingham T.E. Human infrapatellar fat pad-derived stem cells express the pericyte marker 3G5 and show enhanced chondrogenesis after expansion in fibroblast growth factor-2. Arthritis Res Ther. 2008;10(4):10-17. doi.org/10.1186/ar2448
  24. Kon E., Vannini F., Buda R., Filardo G., Cavallo M., Ruffilli A., Nanni M., Di Martino A., Marcacci M., Giannini S. How to treat osteochondritis dissecans of the knee: surgical techniques and new trends: AAOS exhibit selection. J Bone Joint Surg Am. 2012;94:1-8. doi.org/10.2106/jbjs.k.00748
  25. Koh Y.G., Kwon O.R., Kim Y.S., Choi Y.J., Tak D.H. Adipose-derived mesenchymal stem cells with microfracture versus microfracture alone: 2-year follow-up of a prospective randomized trial. Arthroscopy. 2016;32(1):97-109.
  26. Kon E., Filardo G., Berruto M., Benazzo F., Zanon G., Della Villa S., Marcacci M. Articular cartilage treatment in high-level male soccer players: a prospective comparative study of arthroscopic second-generation autologous chondrocyte implantation versus microfracture. Am J Sports Med.2011; 39:2549-2557. doi.org/10.1177/0363546511420688
  27. Kuroda R., Ishida K., Matsumoto T., Akisue T., Fujioka H., Mizuno K., Ohgushi H., Wakitani S., Kurosaka M. Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. Osteoarthritis Cartilage. 2007;15: 226-231. doi.org/10.1016/j.joca.2006.08.008
  28. Kuroda R., Ishida K., Matsumoto T., Akisue T., Fujioka H., Mizuno K., Ohgushi H., Wakitani S., Kurosaka M. Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. Osteoarthritis Cartilage. 2011;17(2): 219-227. doi.org/10.1089/ten.tec.2010.0200
  29. Kafienah W., Mistry S., Dickinson SC., Sims TJ., Learmonth I., Hollander A.P. Three-dimensional cartilage tissue engineering using adult stem cells from osteoarthritis patients. Arthritis Rheum. 2007;56:177-187. doi.org/10.1016/s1063-4584(07)61356-9
  30. Li Q., Tang J., Wang R., Bei C., Xin L., Zeng Y., Tang X. Comparing the chondrogenic potential in vivo of autogeneic mesenchymal stem cells derived from different tissues. Artif Cells Blood Substit Immobil Biotechnol. 2010; 39:31-38. doi.org/10.3109/10731191003776769
  31. Liao Y.H., Chang Y.H., Sung L.Y., Li K.C., Yeh C.L., Yen T.C., Hwang S.M., Lin K.J., Hu Y.C. Osteogenic differentiation of adipose-derived stem cells and calvarial defect repair using baculovirus-mediated co-expression of BMP-2 and miR-148b. Biomaterials. 2014;35(18):4901-4910. doi.org/10.1016/j.biomaterials.2014.02.055
  32. Makris E.A., Gomoll A.H., Malizos K.N., Hu J.C., Athanasiou K.A. Repair and tissue engineering techniques for articular cartilage. Nat Rev Rheumatol. 2014;11(1):21-34. doi.org/10.1038/nrrheum.2014.157
  33. Madry H., Orth P., Kaul G., Zurakowski D., Menger M.D., Kohn D., Cucchiarini M. Acceleration of articular cartilage repair by combined gene transfer of human insulin-like growth factor I and fibroblast growth factor-2 in vivo. Arch Orthop Trauma Surg, 2010;130(10):1311-1322. doi.org/10.1007/s00402-010-1130-3
  34. Martin I., Muraglia A., Campanile G., Cancedda R., Quarto R. Fibroblast growth factor-2 supports ex vivo expansion and maintenance of osteogenic precursors from human bone marrow. Endocrinology. 1997;138:4456-4462. doi: 10.1210/endo.138.10.5425
  35. Martinez I., ElvenesJ .,OlsenR., BertheussenK.,Johansen O. Redifferentiation of in vitro expanded adult articular chondrocytes by combining the hanging-drop cultivation method with hypoxic environment. Cell Transplant. 2008;17:987-996. doi.org/10.3727/096368908786576499
  36. Marlovits S., Hombauer M., Truppe M., Vecsei V., Schlegel W. Changes in the ratio of type-I and type-II collagen expression during monolayer culture of human chondrocytes. J Bone Joint Surg Br. 2004;86(2):286-295. doi.org/10.1302/0301-620x.86b2.14918
  37. Murphy J.M., Marloes L., de Vries-van Melle M.L., Narcisi R., Kops N., Koevoet W.J., Bos PK., Verhaar J.A., van der Kraan P.M., van Osch G.J. Chondrogenesis of mesenchymal stem cells in an osteochondral environment
  38. Marquass В., Schulz R., Hepp P., Zscharnack M., Aigner T., Schmidt S., Stein F., Richter R., Osterhoff G., Aust G., Josten C., Bader A. Matrix-associated implantation of predifferentiated mesenchymal stem cells versus articular chondrocytes: in vivo results of cartilage repair after 1 year. Am J Sports Med. 2011;39:1401-1412. doi.org/10.1177/0363546511398646
  39. Matsuda C., Takagi M., Hattori T., Wakitani S., Yoshida T. Differentiation of human bone marrow mesenchymal stem cells to chondrocytes for construction of three-dimensional cartilage tissue. Cytotechnology. 2005;47: 11-17. doi.org/10.1007/s10616-005-3751-x
  40. Mobasheri A., Kalamegam G., Musumeci G., Batt M.E. Chondrocyte and mesenchymal stem cell-based therapies for cartilage repair in osteoarthritis and related orthopaedic conditions. Maturitas. 2014;78(3):188-198. doi.org/10.1016/j.maturitas.2014.04.017
  41. Mukonoweshuro В., Brown C.J., Fisher J., Ingham E. Immunogenicity of undifferentiated and differentiated allogeneic mouse mesenchymal stem cells. J Tissue Eng. 2014;5:1-15. doi.org/10.1177/2041731414534255
  42. Naderi-Meshkin H., Andreas K., Matin MM., Sittinger M., Bidkhori H.R., Ahmadiankia N., Bahrami A.R., Ringe J. Chitosan-based injectable hydrogel as a promising in situ forming scaffold for cartilage tissue engineering. Cell Biol Int. 2013;38(1):72-84. doi.org/10.1002/cbin.10181
  43. Neumann A.J., Alini M., Archer C.W., Stoddart M.J. Chondrogenesis of human bone marrow-derived mesenchymal stem cells is modulated by complex mechanical stimulation and adenoviral-mediated overexpression of bone morphogenetic protein 2. Tissue Eng Part A. 2013;11-19. doi.org/10.1089/ten. tea.2012.0411
  44. Ochi M., Uchio Y., Tobita M., Kuriwaka M. Current concepts in tissue engineering technique for repair of cartilage defect. Artificial Organs. 2001;25(3):172-179. doi.org/10.1046/j.1525-1594.2001.025003172.x
  45. Pittenger MF., Mackay AM., Beck SC., Jaiswal RK., Douglas R., Mosca JD., Moorman MA., Simonetti DW., Craig S., Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143-147. doi.org/10.1126/science.284.5411.143
  46. Raisin S., Belamie E., Morille M. Non-viral gene activated matricesformesenchymal stemcellsbased tissueengineering of bone and cartilage. Biomaterials. 2016(21);104:223-237. doi.org/10.1016/j.biomaterials.2016.07.017
  47. Sakaguchi Y., Sekiya I., Yagishita K., Muneta T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum. 2005;52(8):2521-2529. doi.org/10.1002/art.21212
  48. Saris D.B. et al. Characterized chondrocyte implantation results in better structural repair when treating symptomatic cartilage defects of the knee in a randomized controlled trial versus microfracture. Am J Sports Med. 2008;36:235-246. doi.org/10.1177/0363546507311095
  49. Saw K.Y., Anz A., Merican S., Tay Y., Ragavanaidu K., Jee C., McGuire D. Articular cartilage regeneration with autologous peripheral blood progenitor cells and hyaluronic acid after arthroscopic subchondral drilling: a report of 5 cases with histology. Arthroscopy. 2011;27: 493-506. doi.org/10.1016/j.arthro.2010.11.054
  50. Saw K.Y., Anz A., Siew-Yoke Jee C., Merican S., Ching-Soong R., Roohi S.A., Ragavanaidu K. Articular cartilage regeneration with autologous peripheral blood stem cells versus hyaluronic acid: a randomized controlled trial. Arthroscopy. 2013;29:684-694. doi.org/10.1016/j. arthro.2012.12.008
  51. Sciaretta F.V. 5 to 8 years follow-up of knee chondral defects treated by PVA-H hydrogel implants. Eur Rev Med Pharmacol Sci. 2013;(17):3031-3038.
  52. Shimomura K., Ando W., Tateishi K., Nansai R., Fujie H., Hart D.A., Kohda H., Kita K., Kanamoto T., Mae T., Nakata K., Shino K., Yoshikawa H., Nakamura N. The influence of skeletal maturity on allogenic synovial mesenchymal stem cell-based repair of cartilage in a large animal model. Biomaterials. 2010;31:8004-8011. doi.org/10.1016/j.biomaterials.2010.07.017
  53. Steinwachs M., Peterson L., Bobic V., Verdonk P., Niemeyer P. Cell-seeded collagen matrix-supported autologous chondrocyte transplantation (ACT-CS): a consensus statement on surgical technique. Cartilage. 2012;3(1):5-12. doi.org/10.1177/1947603511415839
  54. Sun J., Zhong N., Li Q., Min Z., Zhao W., Sun Q., Tian L., Yu H., Shi Q., Zhang F., Lu S. MicroRNAs of rat articular cartilage at different developmental stages identified by Solexa sequencing. Osteoarthritis Cartilage. 2011;19(10): 1237-1245. doi.org/10.1016/j.joca.2011.07.002
  55. Stokes D.G., Liu G., Dharmavaram R., Hawkins D., Piera-Velazquez S., Jimenez S.A. Regulation of type-II collagen gene expression during human chondrocyte de-differentiation and recovery of chondrocyte-specific phenotype in culture involves Sry-type high-mobility-group box (SOX) transcription factors. Biochem J. 2001; 360(Pt2):461-470. doi.org/10.1042/bj3600461
  56. Strappe P., Gurusinghe S. Gene modification of mesenchymal stem cells and articular chondrocytes to enhance chondrogenesis. Biomed Res Int. 2014; 369528: doi: 10.1155/2014/369528
  57. Teo B.J, Buhary K., Tai B.C., Hui J.H. Cell-based therapy improves function in adolescents and young adults with patellar osteochondritis dissecans. Clin Orthop Relat Res. 2012;471(4):1152-1158. doi.org/10.1007/s11999-012-2338-z
  58. Uematsu K., Hattori K., Ishimoto Y., Yamauchi J., Habata T., Takakura Y., Ohgushi H., Fukuchi T., Sato M. Cartilage regeneration using mesenchymal stem cells and a three-dimensional poly-lactic-glycolic acid (PLGA) scaffold. Biomaterials. 2005;26:4273-4279. doi.org/10.1016/j.biomaterials.2004.10.037
  59. Vasiliadis H.S., Danielson В., Ljungberg M., McKeon В., Lindahl A., Peterson L. Implantation of autologous chondrocytes for cartilagenous lesions in young patients. Am J Sports Med. 2010;38(5):943-949.
  60. Wakitani S., Goto T., Pineda S.J., Young R.G., Mansour J.M., Caplan A.I., Goldberg V.M. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am. 1994;76(4): 579-592.
  61. Wakitani S., Imoto K., Yamamoto T., Saito M., Murata N., Yoneda M. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage. 2002;10:199-206. doi.org/10.1053/joca.2001.0504
  62. Wakitani S., Nawata M., Tensho K., Okabe T., Machida H., Ohgushi H. Repair of articular cartilage defects in the patello-femoral joint with autologous bone marrow mesenchymal cell transplantation: three case reports involving nine defects in five knees. J Tissue Eng Regen Med. 2007;1:74-79. doi.org/10.1002/term.8
  63. Wataru Ando, Hiromichi Fujie, Yu Moriguchi, Hideki Yoshikawa, Norimasa Nakamura. Detection of abnormalities in the superficial zone of cartilage repaired using a tissue engineered construct derived from synovial stem cells. Eur Cell Mater. 2012;24.292-307. doi.org/10.1016/j.jbiomech.2015.10.015
  64. Wayne J.S., McDowell C.L., Shields K.J., Tuan R.S. In vivo response of polylactic acid-alginate scaffolds and bone marrow-derived cells for cartilage tissue engineering. Tissue Eng. 2005;11:953-963. doi.org/10.1089/ten.2005.11.953
  65. Yan C., Wang Y., Shen XY., Yang G., Jian J., Wang HS., Chen GQ., Wu Q. MicroRNA regulation associated chondrogenesis of mouse MSCs grown on polyhydroxyalkanoates. Biomaterials. 2011;32(27):6435-6444. doi.org/10.1016/j.biomaterials.2011.05.031
  66. Yu-Chen Hu. Therapy for cartilage and bone tissue engineering. Heidelberg : Springer; 2014. 89 р. doi.org/10.1007/978-3-642-53923-7
  67. Zhao Y.H., Yang Q., Xia Q., Peng J., Lu S.B., Guo Q.Y., Ma X.L., Xu B.S., Hu Y.C., Zhao В., Zhang L., Wang A.Y., Xu W.J., Miao J., Liu Y. In vitro cartilage production using an extracellular matrix-derived scaffold and bone marrow-derived mesenchymal stem cells. Chin Med J (Engl). 2013; 126:3130-3137. doi.org/10.1007/s12015-013-9456-1
  68. Zeifang F., Oberle D., Nierhoff C., Richter W., Moradi В., Schmitt H. Autologous chondrocyte implantation using the original periosteum-cover technique versus matrix-associated autologous chondrocyte implantation: a randomized clinical trial. Am J Sports Med. 2009; 38(5): 924-933. doi.org/10.1177/0363546509351499

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