Research progress of nanomaterials for intra-articular targeted drug delivery in treatment of osteoarthritis_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZONG Lujie ¹ , WU Qian ^1,2 , DONG Zhongchen ¹ , HUANG Lixin ¹ ,  YANG Huilin ¹

1. Department of Orthopedics, the First Affiliated Hospital of Soochow University, Suzhou Jiangsu, 215000, P. R. China;
2. Department of Orthopedics, the First People’s Hospital of Kunshan, Kunshan Jiangsu, 215300, P. R. China;

Corresponding author：

YANG Huilin, Email: yanghlsz@163.com

Keywords：

Osteoarthritis; intra-articular injection; nanomaterials; targeted delivery

DOI：

10.7507/1002-1892.202203033

Video：

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Objective To review the research progress of intra-articular targeted delivery of nanomaterials in the treatment of osteoarthritis (OA). Methods The domestic and foreign related literature on intra-articular targeted delivery of nanomaterials for the treatment of OA was extensively reviewed, and their targeting strategies were discussed and summarized. Results Rapid drug clearance from the joint remains a critical limitation in drug efficacy. Nanocarriers can not only significantly improve the residence profiles of drugs in the joint, but also achieve targeted delivery of drugs to specific joint tissues through active or passive targeting strategies. Conclusion With the continuous development of various emerging tissue- or cell-specific drugs, the targeted delivery of drugs with nanomaterials promise to realize the clinical translation of these drugs in the treatment of OA.

Citation： ZONG Lujie, WU Qian, DONG Zhongchen, HUANG Lixin, YANG Huilin. Research progress of nanomaterials for intra-articular targeted drug delivery in treatment of osteoarthritis. Chinese Journal of Reparative and Reconstructive Surgery, 2022, 36(7): 908-914. doi: 10.7507/1002-1892.202203033 Copy

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2.	Kotlarz H, Gunnarsson CL, Fang H, et al. Insurer and out-of-pocket costs of osteoarthritis in the US: evidence from national survey data. Arthritis Rheum, 2009, 60(12): 3546-3553.
3.	Sharma L. Osteoarthritis of the knee. N Engl J Med, 2021, 384(1): 51-59.
4.	Hunter DJ, Bierma-Zeinstra S. Osteoarthritis. Lancet, 2019, 393(10182): 1745-1759.
5.	Jones IA, Togashi R, Wilson ML, et al. Intra-articular treatment options for knee osteoarthritis. Nat Rev Rheumatol, 2019, 15(2): 77-90.
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9.	Wallis WJ, Simkin PA, Nelp WB. Protein traffic in human synovial effusions. Arthritis Rheum, 1987, 30(1): 57-63.
10.	Edwards SH. Intra-articular drug delivery: the challenge to extend drug residence time within the joint. Vet J, 2011, 190(1): 15-21.
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52.	Cho H, Pinkhassik E, David V, et al. Detection of early cartilage damage using targeted nanosomes in a post-traumatic osteoarthritis mouse model. Nanomedicine, 2015, 11(4): 939-946.
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1. 薛庆云, 王坤正, 裴福兴, 等. 中国40岁以上人群原发性骨关节炎患病状况调查. 中华骨科杂志, 2015, 35(12): 1206-1212.
2. Kotlarz H, Gunnarsson CL, Fang H, et al. Insurer and out-of-pocket costs of osteoarthritis in the US: evidence from national survey data. Arthritis Rheum, 2009, 60(12): 3546-3553.
3. Sharma L. Osteoarthritis of the knee. N Engl J Med, 2021, 384(1): 51-59.
4. Hunter DJ, Bierma-Zeinstra S. Osteoarthritis. Lancet, 2019, 393(10182): 1745-1759.
5. Jones IA, Togashi R, Wilson ML, et al. Intra-articular treatment options for knee osteoarthritis. Nat Rev Rheumatol, 2019, 15(2): 77-90.
6. Larsen C, Ostergaard J, Larsen SW, et al. Intra-articular depot formulation principles: role in the management of postoperative pain and arthritic disorders. J Pharm Sci, 2008, 97(11): 4622-4654.
7. Bijlsma JW, Berenbaum F, Lafeber FP. Osteoarthritis: an update with relevance for clinical practice. Lancet, 2011, 377(9783): 2115-2126.
8. Gerwin N, Hops C, Lucke A. Intraarticular drug delivery in osteoarthritis. Adv Drug Deliv Rev, 2006, 58(2): 226-242.
9. Wallis WJ, Simkin PA, Nelp WB. Protein traffic in human synovial effusions. Arthritis Rheum, 1987, 30(1): 57-63.
10. Edwards SH. Intra-articular drug delivery: the challenge to extend drug residence time within the joint. Vet J, 2011, 190(1): 15-21.
11. Zhao F, Zhao Y, Liu Y, et al. Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. Small, 2011, 7(10): 1322-1337.
12. Charron DM, Chen J, Zheng G. Theranostic lipid nanoparticles for cancer medicine. Cancer Treat Res, 2015, 166: 103-127.
13. Mendes M, Sousa JJ, Pais A, et al. Targeted theranostic nanoparticles for brain tumor treatment. Pharmaceutics, 2018, 10(4): 181. doi: 10.3390/pharmaceutics10040181.
14. Ferrari M, Onuoha SC, Pitzalis C. Trojan horses and guided missiles: targeted therapies in the war on arthritis. Nat Rev Rheumatol, 2015, 11(6): 328-337.
15. Kavanaugh TE, Werfel TA, Cho H, et al. Particle-based technologies for osteoarthritis detection and therapy. Drug Deliv Transl Res, 2016, 6(2): 132-147.
16. Cipollaro L, Trucillo P, Bragazzi NL, et al. Liposomes for intra-articular analgesic drug delivery in orthopedics: State-of-art and future perspectives. insights from a systematic mini-review of the literature. Medicina (Kaunas), 2020, 56(9): 423. doi: 10.3390/medicina56090423.
17. Danhier F, Ansorena E, Silva JM, et al. PLGA-based nanoparticles: an overview of biomedical applications. J Control Release, 2012, 161(2): 505-522.
18. Wang D, Miller SC, Liu XM, et al. Novel dexamethasone-HPMA copolymer conjugate and its potential application in treatment of rheumatoid arthritis. Arthritis Res Ther, 2007, 9(1): R2. doi: 10.1186/ar2106.
19. Alam MM, Han HS, Sung S, et al. Endogenous inspired biomineral-installed hyaluronan nanoparticles as pH-responsive carrier of methotrexate for rheumatoid arthritis. J Control Release, 2017, 252: 62-72.
20. Janssen M, Mihov G, Welting T, et al. Drugs and polymers for delivery systems in OA joints: Clinical needs and opportunities. Polymers, 2014, 6(3): 799-819.
21. Daheshia M, Yao JQ. The interleukin 1beta pathway in the pathogenesis of osteoarthritis. J Rheumatol, 2008, 35(12): 2306-2312.
22. Jahn S, Seror J, Klein J. Lubrication of articular cartilage. Annu Rev Biomed Eng, 2016, 18: 235-258.
23. Rosenberg JH, Rai V, Dilisio MF, et al. Damage-associated molecular patterns in the pathogenesis of osteoarthritis: potentially novel therapeutic targets. Mol Cell Biochem, 2017, 434(1-2): 171-179.
24. Wang T, He C. Pro-inflammatory cytokines: The link between obesity and osteoarthritis. Cytokine Growth Factor Rev, 2018, 44: 38-50.
25. Loeser RF, Goldring SR, Scanzello CR, et al. Osteoarthritis: a disease of the joint as an organ. Arthritis Rheum, 2012, 64(6): 1697-1707.
26. DiDomenico CD, Lintz M, Bonassar LJ. Molecular transport in articular cartilage-what have we learned from the past 50 years? Nat Rev Rheumatol, 2018, 14(7): 393-403.
27. Rothenfluh DA, Bermudez H, O’Neil CP, et al. Biofunctional polymer nanoparticles for intra-articular targeting and retention in cartilage. Nat Mater, 2008, 7(3): 248-254.
28. Yan H, Duan X, Pan H, et al. Suppression of NF-κB activity via nanoparticle-based siRNA delivery alters early cartilage responses to injury. Proc Natl Acad Sci U S A, 2016, 113(41): E6199-E6208.
29. Torzilli PA, Arduino JM, Gregory JD, et al. Effect of proteoglycan removal on solute mobility in articular cartilage. J Biomech, 1997, 30(9): 895-902.
30. Elsaid KA, Ferreira L, Truong T, et al. Pharmaceutical nanocarrier association with chondrocytes and cartilage explants: influence of surface modification and extracellular matrix depletion. Osteoarthritis Cartilage, 2013, 21(2): 377-384.
31. Shapiro EM, Borthakur A, Gougoutas A, et al. 23Na MRI accurately measures fixed charge density in articular cartilage. Magn Reson Med, 2002, 47(2): 284-291.
32. Bajpayee AG, Quadir MA, Hammond PT, et al. Charge based intra-cartilage delivery of single dose dexamethasone using Avidin nano-carriers suppresses cytokine-induced catabolism long term. Osteoarthritis Cartilage, 2016, 24(1): 71-81.
33. Freedman JD, Lusic H, Snyder BD, et al. Tantalum oxide nanoparticles for the imaging of articular cartilage using X-ray computed tomography: visualization of ex vivo/in vivo murine tibia and ex vivo human index finger cartilage. Angew Chem Int Ed Engl, 2014, 53(32): 8406-8410.
34. Brown S, Pistiner J, Adjei IM, et al. Nanoparticle properties for delivery to cartilage: the implications of disease state, synovial fluid, and off-target uptake. Mol Pharm, 2019, 16(2): 469-479.
35. Buckwalter JA, Mankin H, Grodzinsky A. Articular cartilage and osteoarthritis. Instr Course Lect, 2005, 54: 465-480.
36. Kang ML, Ko JY, Kim JE, et al. Intra-articular delivery of kartogenin-conjugated chitosan nano/microparticles for cartilage regeneration. Biomaterials, 2014, 35(37): 9984-9994.
37. te Boekhorst BC, Jensen LB, Colombo S, et al. MRI-assessed therapeutic effects of locally administered PLGA nanoparticles loaded with anti-inflammatory siRNA in a murine arthritis model. J Control Release, 2012, 161(3): 772-780.
38. Ha CW, Cho JJ, Elmallah RK, et al. A multicenter, single-blind, phase Ⅱa clinical trial to evaluate the efficacy and safety of a cell-mediated gene therapy in degenerative knee arthritis patients. Hum Gene Ther Clin Dev, 2015, 26(2): 125-130.
39. Chongchai A, Waramit S, Wongwichai T, et al. Targeting human osteoarthritic chondrocytes with ligand directed bacteriophage-based particles. Viruses, 2021, 13(12): 2343. doi: 10.3390/v13122343.
40. Li Y, Wang Y, Chubinskaya S, et al. Effects of insulin-like growth factor-1 and dexamethasone on cytokine-challenged cartilage: relevance to post-traumatic osteoarthritis. Osteoarthritis Cartilage, 2015, 23(2): 266-274.
41. Augustyniak E, Trzeciak T, Richter M, et al. The role of growth factors in stem cell-directed chondrogenesis: a real hope for damaged cartilage regeneration. Int Orthop, 2015, 39(5): 995-1003.
42. Jain A, Mishra SK, Vuddanda PR, et al. Targeting of diacerein loaded lipid nanoparticles to intra-articular cartilage using chondroitin sulfate as homing carrier for treatment of osteoarthritis in rats. Nanomedicine, 2014, 10(5): 1031-1040.
43. Johnson K, Zhu S, Tremblay MS, et al. A stem cell-based approach to cartilage repair. Science, 2012, 336(6082): 717-721.
44. Liu J, Khalil RA. Matrix metalloproteinase inhibitors as investigational and therapeutic tools in unrestrained tissue remodeling and pathological disorders. Prog Mol Biol Transl Sci, 2017, 148: 355-420.
45. Chen Z, Chen J, Wu L, et al. Hyaluronic acid-coated bovine serum albumin nanoparticles loaded with brucine as selective nanovectors for intra-articular injection. Int J Nanomedicine, 2013, 8: 3843-3853.
46. Pi Y, Zhang X, Shi J, et al. Targeted delivery of non-viral vectors to cartilage in vivo using a chondrocyte-homing peptide identified by phage display. Biomaterials, 2011, 32(26): 6324-6332.
47. Ouyang Z, Tan T, Liu C, et al. Targeted delivery of hesperetin to cartilage attenuates osteoarthritis by bimodal imaging with Gd₂(CO₃)₃@PDA nanoparticles via TLR-2/NF-κB/Akt signaling. Biomaterials, 2019, 205: 50-63.
48. Pi Y, Zhang X, Shao Z, et al. Intra-articular delivery of anti-Hif-2α siRNA by chondrocyte-homing nanoparticles to prevent cartilage degeneration in arthritic mice. Gene Ther, 2015, 22(6): 439-448.
49. Mao H, Kawazoe N, Chen G. Cellular uptake of single-walled carbon nanotubes in 3D extracellular matrix-mimetic composite collagen hydrogels. J Nanosci Nanotechnol, 2014, 14(3): 2487-2492.
50. Singh A, Corvelli M, Unterman SA, et al. Enhanced lubrication on tissue and biomaterial surfaces through peptide-mediated binding of hyaluronic acid. Nat Mater, 2014, 13(10): 988-995.
51. Cho H, Stuart JM, Magid R, et al. Theranostic immunoliposomes for osteoarthritis. Nanomedicine, 2014, 10(3): 619-627.
52. Cho H, Pinkhassik E, David V, et al. Detection of early cartilage damage using targeted nanosomes in a post-traumatic osteoarthritis mouse model. Nanomedicine, 2015, 11(4): 939-946.
53. Cho H, Kim BJ, Park SH, et al. Noninvasive visualization of early osteoarthritic cartilage using targeted nanosomes in a destabilization of the medial meniscus mouse model. Int J Nanomedicine, 2018, 13: 1215-1224.
54. Berenbaum F. Osteoarthritis as an inflammatory disease (osteoarthritis is not osteoarthrosis!). Osteoarthritis Cartilage, 2013, 21(1): 16-21.
55. Mathiessen A, Conaghan PG. Synovitis in osteoarthritis: current understanding with therapeutic implications. Arthritis Res Ther, 2017, 19(1): 18. doi: 10.1186/s13075-017-1229-9.
56. Knight AD, Levick JR. Morphometry of the ultrastructure of the blood-joint barrier in the rabbit knee. Q J Exp Physiol, 1984, 69(2): 271-288.
57. Prieto-Potin I, Largo R, Roman-Blas JA, et al. Characterization of multinucleated giant cells in synovium and subchondral bone in knee osteoarthritis and rheumatoid arthritis. BMC Musculoskelet Disord, 2015, 16: 226. doi: 10.1186/s12891-015-0664-5.
58. Evans CH, Kraus VB, Setton LA. Progress in intra-articular therapy. Nat Rev Rheumatol, 2014, 10(1): 11-22.
59. Labens R, Lascelles BD, Charlton AN, et al. Ex vivo effect of gold nanoparticles on porcine synovial membrane. Tissue Barriers, 2013, 1(2): e24314. doi: 10.4161/tisb.24314.
60. Champion JA, Walker A, Mitragotri S. Role of particle size in phagocytosis of polymeric microspheres. Pharm Res, 2008, 25(8): 1815-1821.
61. Horisawa E, Kubota K, Tuboi I, et al. Size-dependency of DL-lactide/glycolide copolymer particulates for intra-articular delivery system on phagocytosis in rat synovium. Pharm Res, 2002, 19(2): 132-139.
62. Barrera P, Blom A, van Lent PL, et al. Synovial macrophage depletion with clodronate-containing liposomes in rheumatoid arthritis. Arthritis Rheum, 2000, 43(9): 1951-1959.
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