Application of tetrahedral framework nucleic acids in the treatment of osteoarthritis_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LI Shuai , SI Haibo ,  SHEN Bin

Orthopedic Research Institute, Department of Orthopedics, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P. R. China;

Corresponding author：

SHEN Bin, Email: shenbin1971@163.com

Keywords：

Tetrahedral framework nucleic acids; microRNA; osteoarthritis; biological vector

DOI：

10.7507/1002-1892.202112054

Video：

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Objective To introduce the characteristics of tetrahedral framework nucleic acids (tFNA), focusing on its application in the treatment of osteoarthritis (OA) and relationship with microRNA (miRNA), and prospect the application of tFNA in the treatment of OA and the new idea of constructing miR-tFNA functional complex to treat OA. Methods Recent studies were extensively reviewed to analyze the mechanism of tFNA and its relationship with OA and miRNA. Results tFNA, a new type of new carrier, can not only play an indirect role in the treatment of OA as a small molecular carrier with therapeutic effect, but also play a direct role through the regulation of chondrocytes. It can bind with the miRNA that can regulate OA. The therapeutic effect of constructing tFNA functional complex loaded with miRNA has been verified in various diseases, and tFNA has advantages compared with other vectors. Conclusion tFNA, a novel framework nucleic acid structure, plays an important role in the treatment of OA. Constructing miR-tFNA functional complex may be an innovative idea in the treatment of OA.

Citation： LI Shuai, SI Haibo, SHEN Bin. Application of tetrahedral framework nucleic acids in the treatment of osteoarthritis. Chinese Journal of Reparative and Reconstructive Surgery, 2022, 36(4): 505-510. doi: 10.7507/1002-1892.202112054 Copy

1.	中华医学会骨科学分会关节外科学组, 中国医师协会骨科医师分会骨关节炎学组, 国家老年疾病临床医学研究中心(湘雅医院), 等. 中国骨关节炎诊疗指南(2021年版). 中华骨科杂志, 2021, 41(18): 1291-1314.
2.	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.
3.	Li S, Tian T, Zhang T, et al. Advances in biological applications of self-assembled DNA tetrahedral nanostructures. Materials Today, 2019, 24: 57-68.
4.	Zhang X, Liu N, Zhou M, et al. DNA nanorobot delivers antisense oligonucleotides silencing c-Met gene expression for cancer therapy. J Biomed Nanotechnol, 2019, 15(9): 1948-1959.
5.	Zhang T, Cui W, Tian T, et al. Progress in biomedical applications of tetrahedral framework nucleic acid-based functional systems. ACS Appl Mater Interfaces, 2020, 12(42): 47115-47126.
6.	Goodman RP, Schaap IA, Tardin CF, et al. Rapid chiral assembly of rigid DNA building blocks for molecular nanofabrication. Science, 2005, 310(5754): 1661-1665.
7.	Zhang X, Liu N, Zhou M, et al. The application of tetrahedral framework nucleic acids as a drug carrier in biomedicine fields. Curr Stem Cell Res Ther, 2021, 16(1): 48-56.
8.	Ma W, Zhan Y, Zhang Y, et al. An intelligent DNA nanorobot with in vitro enhanced protein lysosomal degradation of HER2. Nano Lett, 2019, 19(7): 4505-4517.
9.	Zhao D, Liu M, Li J, et al. Angiogenic aptamer-modified tetrahedral framework nucleic acid promotes angiogenesis in vitro and in vivo. ACS Appl Mater Interfaces, 2021, 13(25): 29439-29449.
10.	Shao X, Cui W, Xie X, et al. Treatment of Alzheimer’s disease with framework nucleic acids. Cell Prolif, 2020, 53(4): e12787. doi: 10.1111/cpr.12787.
11.	Shi S, Fu W, Lin S, et al. Targeted and effective glioblastoma therapy via aptamer-modified tetrahedral framework nucleic acid-paclitaxel nanoconjugates that can pass the blood brain barrier. Nanomedicine, 2019, 21: 102061. doi: 10.1016/j.nano.2019.102061.
12.	Gao S, Li Y, Xiao D, et al. Tetrahedral framework nucleic acids induce immune tolerance and prevent the onset of type 1 diabetes. Nano Lett, 2021, 21(10): 4437-4446.
13.	Liu X, Yu Z, Wu Y, et al. The immune regulatory effects of tetrahedral framework nucleic acid on human T cells via the mitogen-activated protein kinase pathway. Cell Prolif, 2021, 54(8): e13084. doi: 10.1111/cpr.13084.
14.	Shi SR, Chen Y, Tian TR, et al. Effects of tetrahedral framework nucleic acid/wogonin complexes on osteoarthritis. Bone Res, 2020, 8: 6. doi: 10.1038/s41413-019-0077-4.
15.	Shao X, Lin S, Peng Q, et al. Tetrahedral DNA nanostructure: A potential promoter for cartilage tissue regeneration via regulating chondrocyte phenotype and proliferation. Small, 2017, 13(12): 1602770. doi: 10.1002/smll.201602770.
16.	Li P, Fu L, Liao Z, et al. Chitosan hydrogel/3D-printed poly(ε-caprolactone) hybrid scaffold containing synovial mesenchymal stem cells for cartilage regeneration based on tetrahedral framework nucleic acid recruitment. Biomaterials, 2021, 278: 121131. doi: 10.1016/j.biomaterials.2021.121131.
17.	Shi S, Tian T, Li Y, et al. Tetrahedral framework nucleic acid inhibits chondrocyte apoptosis and oxidative stress through activation of autophagy. ACS Appl Mater Interfaces, 2020, 12(51): 56782-56791.
18.	Marmotti A, Bonasia DE, Bruzzone M, et al. Human cartilage fragments in a composite scaffold for single-stage cartilage repair: an in vitro study of the chondrocyte migration and the influence of TGF-β₁ and G-CSF. Knee Surg Sports Traumatol Arthrosc, 2013, 21(8): 1819-1833.
19.	Shi S, Lin S, Shao X, et al. Modulation of chondrocyte motility by tetrahedral DNA nanostructures. Cell Prolif, 2017, 50(5): e12368. doi: 10.1111/cpr.12368.
20.	Marini F, Cianferotti L, Brandi ML. Epigenetic mechanisms in bone biology and osteoporosis: Can they drive therapeutic choices? Int J Mol Sci, 2016, 17(8): 1329. doi: 10.3390/ijms17081329.
21.	Madeira C, Santhagunam A, Salgueiro JB, et al. Advanced cell therapies for articular cartilage regeneration. Trends Biotechnol, 2015, 33(1): 35-42.
22.	Liang Y, Xu X, Li X, et al. Chondrocyte-targeted microRNA delivery by engineered exosomes toward a cell-free osteoarthritis therapy. ACS Appl Mater Interfaces, 2020, 12(33): 36938-36947.
23.	Jin Z, Ren J, Qi S. Exosomal miR-9-5p secreted by bone marrow-derived mesenchymal stem cells alleviates osteoarthritis by inhibiting syndecan-1. Cell Tissue Res, 2020, 381(1): 99-114.
24.	Wang X, Guo Y, Wang C, et al. MicroRNA-142-3p inhibits chondrocyte apoptosis and inflammation in osteoarthritis by targeting HMGB1. Inflammation, 2016, 39(5): 1718-1728.
25.	Zhu H, Yan X, Zhang M, et al. miR-21-5p protects IL-1β-induced human chondrocytes from degradation. J Orthop Surg Res, 2019, 14(1): 118. doi: 10.1186/s13018-019-1160-7.
26.	Zhang Y, Lin J, Zhou X, et al. Melatonin prevents osteoarthritis-induced cartilage degradation via targeting microRNA-140. Oxid Med Cell Longev, 2019, 2019: 9705929. doi: 10.1155/2019/9705929.
27.	Trang P, Wiggins JF, Daige CL, et al. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol Ther, 2011, 19(6): 1116-1122.
28.	Simonson B, Das S. MicroRNA therapeutics: the next magic bullet? Mini Rev Med Chem, 2015, 15(6): 467-474.
29.	Miao P, Wang B, Chen X, et al. Tetrahedral DNA nanostructure-based microRNA biosensor coupled with catalytic recycling of the analyte. ACS Appl Mater Interfaces, 2015, 7(11): 6238-6243.
30.	Zhu D, Wei Y, Sun T, et al. Encoding DNA frameworks for amplified multiplexed imaging of intracellular microRNAs. Anal Chem, 2021, 93(4): 2226-2234.
31.	Wu W, Yu X, Wu J, et al. Surface plasmon resonance imaging-based biosensor for multiplex and ultrasensitive detection of NSCLC-associated exosomal miRNAs using DNA programmed heterostructure of Au-on-Ag. Biosens Bioelectron, 2021, 175: 112835. doi: 10.1016/j.bios.2020.112835.
32.	Yu L, Zhu L, Yan M, et al. Electrochemiluminescence biosensor based on entropy-driven amplification and a tetrahedral DNA nanostructure for miRNA-133a Detection. Anal Chem, 2021, 93(34): 11809-11815.
33.	Li S, Sun Y, Tian T, et al. MicroRNA-214-3p modified tetrahedral framework nucleic acids target survivin to induce tumour cell apoptosis. Cell Prolif, 2020, 53(1): e12708. doi: 10.1111/cpr.12708.
34.	Song G, Dong H, Ma D, et al. Tetrahedral framework nucleic acid delivered RNA therapeutics significantly attenuate pancreatic cancer progression via inhibition of CTR1-dependent copper absorption. ACS Appl Mater Interfaces, 2021, 13(39): 46334-46342.
35.	Li D, Yang Z, Luo Y, et al. Delivery of miR335-5p-pendant tetrahedron DNA nanostructures using an injectable heparin lithium hydrogel for challenging bone defects in steroid-associated osteonecrosis. Adv Healthc Mater, 2022, 11(1): e2101412. doi: 10.1002/adhm.202101412.
36.	Esmaeili A, Hosseini S, Baghaban Eslaminejad M. Engineered-extracellular vesicles as an optimistic tool for microRNA delivery for osteoarthritis treatment. Cell Mol Life Sci, 2021, 78(1): 79-91.
37.	Daniel R, Smith JA. Integration site selection by retroviral vectors: molecular mechanism and clinical consequences. Hum Gene Ther, 2008, 19(6): 557-568.
38.	Kasar S, Salerno E, Yuan Y, et al. Systemic in vivo lentiviral delivery of miR-15a/16 reduces malignancy in the NZB de novo mouse model of chronic lymphocytic leukemia. Genes Immun, 2012, 13(2): 109-119.
39.	Santhagunam A, Madeira C, Cabral JM. Genetically engineered stem cell-based strategies for articular cartilage regeneration. Biotechnol Appl Biochem, 2012, 59(2): 121-131.
40.	Ishida T, Ichihara M, Wang X, et al. Injection of PEGylated liposomes in rats elicits PEG-specific IgM, which is responsible for rapid elimination of a second dose of PEGylated liposomes. J Control Release, 2006, 112(1): 15-25.
41.	Sarker SR, Arai S, Murate M, et al. Evaluation of the influence of ionization states and spacers in the thermotropic phase behaviour of amino acid-based cationic lipids and the transfection efficiency of their assemblies. Int J Pharm, 2012, 422(1-2): 364-373.
42.	Zhang Y, Ma W, Zhu Y, et al. Inhibiting methicillin-resistant staphylococcus aureus by tetrahedral DNA nanostructure-enabled antisense peptide nucleic acid delivery. Nano Lett, 2018, 18(9): 5652-5659.
43.	Xie X, Shao X, Ma W, et al. Overcoming drug-resistant lung cancer by paclitaxel loaded tetrahedral DNA nanostructures. Nanoscale, 2018, 10(12): 5457-5465.
44.	Liu X, Xu Y, Yu T, et al. A DNA nanostructure platform for directed assembly of synthetic vaccines. Nano Lett, 2012, 12(8): 4254-4259.
45.	Chen C, Yang Z, Tang X. Chemical modifications of nucleic acid drugs and their delivery systems for gene-based therapy. Med Res Rev, 2018, 38(3): 829-869.

1. 中华医学会骨科学分会关节外科学组, 中国医师协会骨科医师分会骨关节炎学组, 国家老年疾病临床医学研究中心(湘雅医院), 等. 中国骨关节炎诊疗指南(2021年版). 中华骨科杂志, 2021, 41(18): 1291-1314.
2. 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.
3. Li S, Tian T, Zhang T, et al. Advances in biological applications of self-assembled DNA tetrahedral nanostructures. Materials Today, 2019, 24: 57-68.
4. Zhang X, Liu N, Zhou M, et al. DNA nanorobot delivers antisense oligonucleotides silencing c-Met gene expression for cancer therapy. J Biomed Nanotechnol, 2019, 15(9): 1948-1959.
5. Zhang T, Cui W, Tian T, et al. Progress in biomedical applications of tetrahedral framework nucleic acid-based functional systems. ACS Appl Mater Interfaces, 2020, 12(42): 47115-47126.
6. Goodman RP, Schaap IA, Tardin CF, et al. Rapid chiral assembly of rigid DNA building blocks for molecular nanofabrication. Science, 2005, 310(5754): 1661-1665.
7. Zhang X, Liu N, Zhou M, et al. The application of tetrahedral framework nucleic acids as a drug carrier in biomedicine fields. Curr Stem Cell Res Ther, 2021, 16(1): 48-56.
8. Ma W, Zhan Y, Zhang Y, et al. An intelligent DNA nanorobot with in vitro enhanced protein lysosomal degradation of HER2. Nano Lett, 2019, 19(7): 4505-4517.
9. Zhao D, Liu M, Li J, et al. Angiogenic aptamer-modified tetrahedral framework nucleic acid promotes angiogenesis in vitro and in vivo. ACS Appl Mater Interfaces, 2021, 13(25): 29439-29449.
10. Shao X, Cui W, Xie X, et al. Treatment of Alzheimer’s disease with framework nucleic acids. Cell Prolif, 2020, 53(4): e12787. doi: 10.1111/cpr.12787.
11. Shi S, Fu W, Lin S, et al. Targeted and effective glioblastoma therapy via aptamer-modified tetrahedral framework nucleic acid-paclitaxel nanoconjugates that can pass the blood brain barrier. Nanomedicine, 2019, 21: 102061. doi: 10.1016/j.nano.2019.102061.
12. Gao S, Li Y, Xiao D, et al. Tetrahedral framework nucleic acids induce immune tolerance and prevent the onset of type 1 diabetes. Nano Lett, 2021, 21(10): 4437-4446.
13. Liu X, Yu Z, Wu Y, et al. The immune regulatory effects of tetrahedral framework nucleic acid on human T cells via the mitogen-activated protein kinase pathway. Cell Prolif, 2021, 54(8): e13084. doi: 10.1111/cpr.13084.
14. Shi SR, Chen Y, Tian TR, et al. Effects of tetrahedral framework nucleic acid/wogonin complexes on osteoarthritis. Bone Res, 2020, 8: 6. doi: 10.1038/s41413-019-0077-4.
15. Shao X, Lin S, Peng Q, et al. Tetrahedral DNA nanostructure: A potential promoter for cartilage tissue regeneration via regulating chondrocyte phenotype and proliferation. Small, 2017, 13(12): 1602770. doi: 10.1002/smll.201602770.
16. Li P, Fu L, Liao Z, et al. Chitosan hydrogel/3D-printed poly(ε-caprolactone) hybrid scaffold containing synovial mesenchymal stem cells for cartilage regeneration based on tetrahedral framework nucleic acid recruitment. Biomaterials, 2021, 278: 121131. doi: 10.1016/j.biomaterials.2021.121131.
17. Shi S, Tian T, Li Y, et al. Tetrahedral framework nucleic acid inhibits chondrocyte apoptosis and oxidative stress through activation of autophagy. ACS Appl Mater Interfaces, 2020, 12(51): 56782-56791.
18. Marmotti A, Bonasia DE, Bruzzone M, et al. Human cartilage fragments in a composite scaffold for single-stage cartilage repair: an in vitro study of the chondrocyte migration and the influence of TGF-β₁ and G-CSF. Knee Surg Sports Traumatol Arthrosc, 2013, 21(8): 1819-1833.
19. Shi S, Lin S, Shao X, et al. Modulation of chondrocyte motility by tetrahedral DNA nanostructures. Cell Prolif, 2017, 50(5): e12368. doi: 10.1111/cpr.12368.
20. Marini F, Cianferotti L, Brandi ML. Epigenetic mechanisms in bone biology and osteoporosis: Can they drive therapeutic choices? Int J Mol Sci, 2016, 17(8): 1329. doi: 10.3390/ijms17081329.
21. Madeira C, Santhagunam A, Salgueiro JB, et al. Advanced cell therapies for articular cartilage regeneration. Trends Biotechnol, 2015, 33(1): 35-42.
22. Liang Y, Xu X, Li X, et al. Chondrocyte-targeted microRNA delivery by engineered exosomes toward a cell-free osteoarthritis therapy. ACS Appl Mater Interfaces, 2020, 12(33): 36938-36947.
23. Jin Z, Ren J, Qi S. Exosomal miR-9-5p secreted by bone marrow-derived mesenchymal stem cells alleviates osteoarthritis by inhibiting syndecan-1. Cell Tissue Res, 2020, 381(1): 99-114.
24. Wang X, Guo Y, Wang C, et al. MicroRNA-142-3p inhibits chondrocyte apoptosis and inflammation in osteoarthritis by targeting HMGB1. Inflammation, 2016, 39(5): 1718-1728.
25. Zhu H, Yan X, Zhang M, et al. miR-21-5p protects IL-1β-induced human chondrocytes from degradation. J Orthop Surg Res, 2019, 14(1): 118. doi: 10.1186/s13018-019-1160-7.
26. Zhang Y, Lin J, Zhou X, et al. Melatonin prevents osteoarthritis-induced cartilage degradation via targeting microRNA-140. Oxid Med Cell Longev, 2019, 2019: 9705929. doi: 10.1155/2019/9705929.
27. Trang P, Wiggins JF, Daige CL, et al. Systemic delivery of tumor suppressor microRNA mimics using a neutral lipid emulsion inhibits lung tumors in mice. Mol Ther, 2011, 19(6): 1116-1122.
28. Simonson B, Das S. MicroRNA therapeutics: the next magic bullet? Mini Rev Med Chem, 2015, 15(6): 467-474.
29. Miao P, Wang B, Chen X, et al. Tetrahedral DNA nanostructure-based microRNA biosensor coupled with catalytic recycling of the analyte. ACS Appl Mater Interfaces, 2015, 7(11): 6238-6243.
30. Zhu D, Wei Y, Sun T, et al. Encoding DNA frameworks for amplified multiplexed imaging of intracellular microRNAs. Anal Chem, 2021, 93(4): 2226-2234.
31. Wu W, Yu X, Wu J, et al. Surface plasmon resonance imaging-based biosensor for multiplex and ultrasensitive detection of NSCLC-associated exosomal miRNAs using DNA programmed heterostructure of Au-on-Ag. Biosens Bioelectron, 2021, 175: 112835. doi: 10.1016/j.bios.2020.112835.
32. Yu L, Zhu L, Yan M, et al. Electrochemiluminescence biosensor based on entropy-driven amplification and a tetrahedral DNA nanostructure for miRNA-133a Detection. Anal Chem, 2021, 93(34): 11809-11815.
33. Li S, Sun Y, Tian T, et al. MicroRNA-214-3p modified tetrahedral framework nucleic acids target survivin to induce tumour cell apoptosis. Cell Prolif, 2020, 53(1): e12708. doi: 10.1111/cpr.12708.
34. Song G, Dong H, Ma D, et al. Tetrahedral framework nucleic acid delivered RNA therapeutics significantly attenuate pancreatic cancer progression via inhibition of CTR1-dependent copper absorption. ACS Appl Mater Interfaces, 2021, 13(39): 46334-46342.
35. Li D, Yang Z, Luo Y, et al. Delivery of miR335-5p-pendant tetrahedron DNA nanostructures using an injectable heparin lithium hydrogel for challenging bone defects in steroid-associated osteonecrosis. Adv Healthc Mater, 2022, 11(1): e2101412. doi: 10.1002/adhm.202101412.
36. Esmaeili A, Hosseini S, Baghaban Eslaminejad M. Engineered-extracellular vesicles as an optimistic tool for microRNA delivery for osteoarthritis treatment. Cell Mol Life Sci, 2021, 78(1): 79-91.
37. Daniel R, Smith JA. Integration site selection by retroviral vectors: molecular mechanism and clinical consequences. Hum Gene Ther, 2008, 19(6): 557-568.
38. Kasar S, Salerno E, Yuan Y, et al. Systemic in vivo lentiviral delivery of miR-15a/16 reduces malignancy in the NZB de novo mouse model of chronic lymphocytic leukemia. Genes Immun, 2012, 13(2): 109-119.
39. Santhagunam A, Madeira C, Cabral JM. Genetically engineered stem cell-based strategies for articular cartilage regeneration. Biotechnol Appl Biochem, 2012, 59(2): 121-131.
40. Ishida T, Ichihara M, Wang X, et al. Injection of PEGylated liposomes in rats elicits PEG-specific IgM, which is responsible for rapid elimination of a second dose of PEGylated liposomes. J Control Release, 2006, 112(1): 15-25.
41. Sarker SR, Arai S, Murate M, et al. Evaluation of the influence of ionization states and spacers in the thermotropic phase behaviour of amino acid-based cationic lipids and the transfection efficiency of their assemblies. Int J Pharm, 2012, 422(1-2): 364-373.
42. Zhang Y, Ma W, Zhu Y, et al. Inhibiting methicillin-resistant staphylococcus aureus by tetrahedral DNA nanostructure-enabled antisense peptide nucleic acid delivery. Nano Lett, 2018, 18(9): 5652-5659.
43. Xie X, Shao X, Ma W, et al. Overcoming drug-resistant lung cancer by paclitaxel loaded tetrahedral DNA nanostructures. Nanoscale, 2018, 10(12): 5457-5465.
44. Liu X, Xu Y, Yu T, et al. A DNA nanostructure platform for directed assembly of synthetic vaccines. Nano Lett, 2012, 12(8): 4254-4259.
45. Chen C, Yang Z, Tang X. Chemical modifications of nucleic acid drugs and their delivery systems for gene-based therapy. Med Res Rev, 2018, 38(3): 829-869.

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