Regulation of non-coding RNA in type H vessels angiogenesis of bone_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

TANG Shengping , LIAO Shijie , LIU Jianhong , LUO Xiaolin , WEI Zhendi ,  DING Xiaofei

Department of Trauma Orthopedic and Hand Surgery, the First Affiliated Hospital of Guangxi Medical University, Nanning Guangxi, 530021, P. R. China;

Corresponding author：

DING Xiaofei, Email: dxfeicsgk2014@163.com

Keywords：

Non-coding RNA; type H vessels; angiogenesis; osteogenesis; regulation

DOI：

10.7507/1002-1892.202304032

Video：

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Objective To summarize the regulatory effect of non-coding RNA (ncRNA) on type H vessels angiogenesis of bone. Methods Recent domestic and foreign related literature about the regulation of ncRNA in type H vessels angiogenesis was widely reviewed and summarized. Results Type H vessels is a special subtype of bone vessels with the ability to couple bone formation. At present, the research on ncRNA regulating type H vessels angiogenesis in bone diseases mainly focuses on microRNA, long ncRNA, and small interfering RNA, which can affect the expressions of hypoxia inducible factor 1α, platelet derived growth factor BB, slit guidance ligand 3, and other factors through their own unique ways of action, thus regulating type H vessels angiogenesis and participating in the occurrence and development of bone diseases. Conclusion At present, the mechanism of ncRNA regulating bone type H vessels angiogenesis has been preliminarily explored. With the deepening of research, ncRNA is expected to be a new target for the diagnosis and treatment of vascular related bone diseases.

Citation： TANG Shengping, LIAO Shijie, LIU Jianhong, LUO Xiaolin, WEI Zhendi, DING Xiaofei. Regulation of non-coding RNA in type H vessels angiogenesis of bone. Chinese Journal of Reparative and Reconstructive Surgery, 2023, 37(8): 1042-1048. doi: 10.7507/1002-1892.202304032 Copy

1.	Sivan U, De Angelis J, Kusumbe AP. Role of angiocrine signals in bone development, homeostasis and disease. Open Biol, 2019, 9(10): 190144. doi: 10.1098/rsob.190144.
2.	Peng Y, Wu S, Li Y, et al. Type H blood vessels in bone modeling and remodeling. Theranostics, 2020, 10(1): 426-436.
3.	Yang Y, Yujiao W, Fang W, et al. The roles of miRNA, lncRNA and circRNA in the development of osteoporosis. Biol Res, 2020, 53(1): 40. doi: 10.1186/s40659-020-00309-z.
4.	褚美玲, 陈红风, 殷玉莲, 等. H型血管在改善骨丢失中的作用机制研究进展. 中华骨科杂志, 2022, 42(22): 1523-1530.
5.	Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature, 2014, 507(7492): 323-328.
6.	Wang L, Zhou F, Zhang P, et al. Human type H vessels are a sensitive biomarker of bone mass. Cell Death Dis, 2017, 8(5): e2760. doi: 10.1038/cddis.2017.36.
7.	Zhu Y, Ruan Z, Lin Z, et al. The association between CD31hiEmcnhi endothelial cells and bone mineral density in Chinese women. J Bone Miner Metab, 2019, 37(6): 987-995.
8.	Liu Y, Xie HQ, Shen B. Type H vessels-a bridge connecting subchondral bone remodelling and articular cartilage degeneration in osteoarthritis development. Rheumatology (Oxford), 2023, 62(4): 1436-1444.
9.	Chen X, He W, Sun M, et al. STING inhibition accelerates the bone healing process while enhancing type H vessel formation. FASEB J, 2021, 35(11): e21964. doi: 10.1096/fj.202100069RR.
10.	Xie H, Cui Z, Wang L, et al. PDGF-BB secreted by preosteoclasts induces angiogenesis during coupling with osteogenesis. Nat Med, 2014, 20(11): 1270-1278.
11.	Xu R, Yallowitz A, Qin A, et al. Targeting skeletal endothelium to ameliorate bone loss. Nat Med, 2018, 24(6): 823-833.
12.	Chen K, Liao S, Li Y, et al. Osteoblast-derived EGFL6 couples angiogenesis to osteogenesis during bone repair. Theranostics, 2021, 11(20): 9738-9751.
13.	Guan S, Zhang Z, Wu J. Non-coding RNA delivery for bone tissue engineering: Progress, challenges, and potential solutions. iScience, 2022, 25(8): 104807. doi: 10.1016/j.isci.2022.104807.
14.	Bellavia D, Salamanna F, Raimondi L, et al. Deregulated miRNAs in osteoporosis: effects in bone metastasis. Cell Mol Life Sci, 2019, 76(19): 3723-3744.
15.	王亮, 顾剑, 赵宇, 等. 髋部骨折患者骨内H型血管的变化. 中华骨质疏松和骨矿盐疾病杂志, 2020, 13(6): 516-521.
16.	陈赛楠, 黄云梅, 林燕萍, 等. miR-148-5p靶向H型血管调控因子Slit3的实验研究. 中国骨质疏松杂志, 2022, 28(7): 959-965.
17.	Wang X, Li X, Li J, et al. Mechanical loading stimulates bone angiogenesis through enhancing type H vessel formation and downregulating exosomal miR-214-3p from bone marrow-derived mesenchymal stem cells. FASEB J, 2021, 35(1): e21150. doi: 10.1096/fj.202001080RR.
18.	He WZ, Yang M, Jiang Y, et al. miR-188-3p targets skeletal endothelium coupling of angiogenesis and osteogenesis during ageing. Cell Death Dis, 2022, 13(5): 494. doi: 10.1038/s41419-022-04902-w.
19.	Lu J, Zhang H, Cai D, et al. Positive-feedback regulation of subchondral H-type vessel formation by chondrocyte promotes osteoarthritis development in mice. J Bone Miner Res, 2018, 33(5): 909-920.
20.	Wang R, Xu B. TGFβ₁-modified MSC-derived exosome attenuates osteoarthritis by inhibiting PDGF-BB secretion and H-type vessel activity in the subchondral bone. Acta Histochem, 2022, 124(7): 151933. doi: 10.1016/j.acthis.2022.151933.
21.	Wood J, Bonjean K, Ruetz S, et al. Novel antiangiogenic effects of the bisphosphonate compound zoledronic acid. J Pharmacol Exp Ther, 2002, 302(3): 1055-1061.
22.	Yan ZQ, Wang XK, Zhou Y, et al. H-type blood vessels participate in alveolar bone remodeling during murine tooth extraction healing. Oral Dis, 2020, 26(5): 998-1009.
23.	Shen X, Zhu W, Zhang P, et al. Macrophage miR-149-5p induction is a key driver and therapeutic target for BRONJ. JCI Insight, 2022, 7(16): e159865. doi: 10.1172/jci.insight.159865.
24.	He H, Luo H, Liu L, et al. Prenatal caffeine exposure caused H-type blood vessel-related long bone dysplasia via miR375/CTGF signaling. FASEB J, 2021, 35(2): e21370. doi: 10.1096/fj.202002230R.
25.	Yang M, Li CJ, Sun X, et al. MiR-497~195 cluster regulates angiogenesis during coupling with osteogenesis by maintaining endothelial Notch and HIF-1α activity. Nat Commun, 2017, 8: 16003. doi: 10.1038/ncomms16003.
26.	Dou C, Zhang C, Kang F, et al. MiR-7b directly targets DC-STAMP causing suppression of NFATc1 and c-Fos signaling during osteoclast fusion and differentiation. Biochim Biophys Acta, 2014, 1839(11): 1084-1096.
27.	Dou C, Ding N, Luo F, et al. Graphene-based microRNA transfection blocks preosteoclast fusion to increase bone formation and vascularization. Adv Sci (Weinh), 2017, 5(2): 1700578. doi: 10.1002/advs.201700578.
28.	Chen Y, Yu H, Zhu D, et al. miR-136-3p targets PTEN to regulate vascularization and bone formation and ameliorates alcohol-induced osteopenia. FASEB J, 2020, 34(4): 5348-5362.
29.	Wang R, Zhang H, Ding W, et al. miR-143 promotes angiogenesis and osteoblast differentiation by targeting HDAC7. Cell Death Dis, 2020, 11(3): 179. doi: 10.1038/s41419-020-2377-4.
30.	Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev, 2009, 23(13): 1494-1504.
31.	Leupin O, Piters E, Halleux C, et al. Bone overgrowth-associated mutations in the LRP4 gene impair sclerostin facilitator function. J Biol Chem, 2011, 286(22): 19489-19500.
32.	Yang M, Guo Q, Peng H, et al. Krüppel-like factor 3 inhibition by mutated lncRNA Reg1cp results in human high bone mass syndrome. J Exp Med, 2019, 216(8): 1944-1964.
33.	Yang M, Li CJ, Xiao Y, et al. Ophiopogonin D promotes bone regeneration by stimulating CD31hi EMCNhi vessel formation. Cell Prolif, 2020, 53(3): e12784. doi: 10.1111/cpr.12784.
34.	Ma Q, Liang M, Limjunyawong N, et al. Osteoclast-derived apoptotic bodies show extended biological effects of parental cell in promoting bone defect healing. Theranostics, 2020, 10(15): 6825-6838.
35.	Bai Y, Gong X, Dong R, et al. Long non-coding RNA HCAR promotes endochondral bone repair by upregulating VEGF and MMP13 in hypertrophic chondrocyte through sponging miR-15b-5p. Genes Dis, 2020, 9(2): 456-465.
36.	Alshaer W, Zureigat H, Al Karaki A, et al. siRNA: Mechanism of action, challenges, and therapeutic approaches. Eur J Pharmacol, 2021, 905: 174178. doi: 10.1016/j.ejphar.2021.174178.
37.	Leng Q, Chen L, Lv Y. RNA-based scaffolds for bone regeneration: application and mechanisms of mRNA, miRNA and siRNA. Theranostics, 2020, 10(7): 3190-3205.
38.	Cui Y, Guo Y, Kong L, et al. A bone-targeted engineered exosome platform delivering siRNA to treat osteoporosis. Bioact Mater, 2021, 10: 207-221.
39.	Liang S, Ling S, Du R, et al. The coupling of reduced type H vessels with unloading-induced bone loss and the protection role of Panax quinquefolium saponin in the male mice. Bone, 2021, 143: 115712. doi: 10.1016/j.bone.2020.115712.
40.	Yang C, Liu Y, Wang Z, et al. Controlled mechanical loading improves bone regeneration by regulating type H vessels in a S1Pr1-dependent manner. FASEB J, 2022, 36(10): e22530. doi: 10.1096/fj.202200339RRR.
41.	Huang J, Li YY, Xia K, et al. Harmine targets inhibitor of DNA binding-2 and activator protein-1 to promote preosteoclast PDGF-BB production. J Cell Mol Med, 2021, 25(12): 5525-5533.
42.	Li Z, Xue H, Tan G, et al. Effects of miRNAs, lncRNAs and circRNAs on osteoporosis as regulatory factors of bone homeostasis (Review). Mol Med Rep, 2021, 24(5): 788. doi: 10.3892/mmr.2021.12428.
43.	Wu W, Lu BF, Jiang RQ, et al. The function and regulation mechanism of piRNAs in human cancers. Histol Histopathol, 2021, 36(8): 807-816.
44.	Hueso M, Mallén A, Suñé-Pou M, et al. ncRNAs in therapeutics: Challenges and limitations in nucleic acid-based drug delivery. Int J Mol Sci, 2021, 22(21): 11596. doi: 10.3390/ijms222111596.

1. Sivan U, De Angelis J, Kusumbe AP. Role of angiocrine signals in bone development, homeostasis and disease. Open Biol, 2019, 9(10): 190144. doi: 10.1098/rsob.190144.
2. Peng Y, Wu S, Li Y, et al. Type H blood vessels in bone modeling and remodeling. Theranostics, 2020, 10(1): 426-436.
3. Yang Y, Yujiao W, Fang W, et al. The roles of miRNA, lncRNA and circRNA in the development of osteoporosis. Biol Res, 2020, 53(1): 40. doi: 10.1186/s40659-020-00309-z.
4. 褚美玲, 陈红风, 殷玉莲, 等. H型血管在改善骨丢失中的作用机制研究进展. 中华骨科杂志, 2022, 42(22): 1523-1530.
5. Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature, 2014, 507(7492): 323-328.
6. Wang L, Zhou F, Zhang P, et al. Human type H vessels are a sensitive biomarker of bone mass. Cell Death Dis, 2017, 8(5): e2760. doi: 10.1038/cddis.2017.36.
7. Zhu Y, Ruan Z, Lin Z, et al. The association between CD31hiEmcnhi endothelial cells and bone mineral density in Chinese women. J Bone Miner Metab, 2019, 37(6): 987-995.
8. Liu Y, Xie HQ, Shen B. Type H vessels-a bridge connecting subchondral bone remodelling and articular cartilage degeneration in osteoarthritis development. Rheumatology (Oxford), 2023, 62(4): 1436-1444.
9. Chen X, He W, Sun M, et al. STING inhibition accelerates the bone healing process while enhancing type H vessel formation. FASEB J, 2021, 35(11): e21964. doi: 10.1096/fj.202100069RR.
10. Xie H, Cui Z, Wang L, et al. PDGF-BB secreted by preosteoclasts induces angiogenesis during coupling with osteogenesis. Nat Med, 2014, 20(11): 1270-1278.
11. Xu R, Yallowitz A, Qin A, et al. Targeting skeletal endothelium to ameliorate bone loss. Nat Med, 2018, 24(6): 823-833.
12. Chen K, Liao S, Li Y, et al. Osteoblast-derived EGFL6 couples angiogenesis to osteogenesis during bone repair. Theranostics, 2021, 11(20): 9738-9751.
13. Guan S, Zhang Z, Wu J. Non-coding RNA delivery for bone tissue engineering: Progress, challenges, and potential solutions. iScience, 2022, 25(8): 104807. doi: 10.1016/j.isci.2022.104807.
14. Bellavia D, Salamanna F, Raimondi L, et al. Deregulated miRNAs in osteoporosis: effects in bone metastasis. Cell Mol Life Sci, 2019, 76(19): 3723-3744.
15. 王亮, 顾剑, 赵宇, 等. 髋部骨折患者骨内H型血管的变化. 中华骨质疏松和骨矿盐疾病杂志, 2020, 13(6): 516-521.
16. 陈赛楠, 黄云梅, 林燕萍, 等. miR-148-5p靶向H型血管调控因子Slit3的实验研究. 中国骨质疏松杂志, 2022, 28(7): 959-965.
17. Wang X, Li X, Li J, et al. Mechanical loading stimulates bone angiogenesis through enhancing type H vessel formation and downregulating exosomal miR-214-3p from bone marrow-derived mesenchymal stem cells. FASEB J, 2021, 35(1): e21150. doi: 10.1096/fj.202001080RR.
18. He WZ, Yang M, Jiang Y, et al. miR-188-3p targets skeletal endothelium coupling of angiogenesis and osteogenesis during ageing. Cell Death Dis, 2022, 13(5): 494. doi: 10.1038/s41419-022-04902-w.
19. Lu J, Zhang H, Cai D, et al. Positive-feedback regulation of subchondral H-type vessel formation by chondrocyte promotes osteoarthritis development in mice. J Bone Miner Res, 2018, 33(5): 909-920.
20. Wang R, Xu B. TGFβ₁-modified MSC-derived exosome attenuates osteoarthritis by inhibiting PDGF-BB secretion and H-type vessel activity in the subchondral bone. Acta Histochem, 2022, 124(7): 151933. doi: 10.1016/j.acthis.2022.151933.
21. Wood J, Bonjean K, Ruetz S, et al. Novel antiangiogenic effects of the bisphosphonate compound zoledronic acid. J Pharmacol Exp Ther, 2002, 302(3): 1055-1061.
22. Yan ZQ, Wang XK, Zhou Y, et al. H-type blood vessels participate in alveolar bone remodeling during murine tooth extraction healing. Oral Dis, 2020, 26(5): 998-1009.
23. Shen X, Zhu W, Zhang P, et al. Macrophage miR-149-5p induction is a key driver and therapeutic target for BRONJ. JCI Insight, 2022, 7(16): e159865. doi: 10.1172/jci.insight.159865.
24. He H, Luo H, Liu L, et al. Prenatal caffeine exposure caused H-type blood vessel-related long bone dysplasia via miR375/CTGF signaling. FASEB J, 2021, 35(2): e21370. doi: 10.1096/fj.202002230R.
25. Yang M, Li CJ, Sun X, et al. MiR-497~195 cluster regulates angiogenesis during coupling with osteogenesis by maintaining endothelial Notch and HIF-1α activity. Nat Commun, 2017, 8: 16003. doi: 10.1038/ncomms16003.
26. Dou C, Zhang C, Kang F, et al. MiR-7b directly targets DC-STAMP causing suppression of NFATc1 and c-Fos signaling during osteoclast fusion and differentiation. Biochim Biophys Acta, 2014, 1839(11): 1084-1096.
27. Dou C, Ding N, Luo F, et al. Graphene-based microRNA transfection blocks preosteoclast fusion to increase bone formation and vascularization. Adv Sci (Weinh), 2017, 5(2): 1700578. doi: 10.1002/advs.201700578.
28. Chen Y, Yu H, Zhu D, et al. miR-136-3p targets PTEN to regulate vascularization and bone formation and ameliorates alcohol-induced osteopenia. FASEB J, 2020, 34(4): 5348-5362.
29. Wang R, Zhang H, Ding W, et al. miR-143 promotes angiogenesis and osteoblast differentiation by targeting HDAC7. Cell Death Dis, 2020, 11(3): 179. doi: 10.1038/s41419-020-2377-4.
30. Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev, 2009, 23(13): 1494-1504.
31. Leupin O, Piters E, Halleux C, et al. Bone overgrowth-associated mutations in the LRP4 gene impair sclerostin facilitator function. J Biol Chem, 2011, 286(22): 19489-19500.
32. Yang M, Guo Q, Peng H, et al. Krüppel-like factor 3 inhibition by mutated lncRNA Reg1cp results in human high bone mass syndrome. J Exp Med, 2019, 216(8): 1944-1964.
33. Yang M, Li CJ, Xiao Y, et al. Ophiopogonin D promotes bone regeneration by stimulating CD31hi EMCNhi vessel formation. Cell Prolif, 2020, 53(3): e12784. doi: 10.1111/cpr.12784.
34. Ma Q, Liang M, Limjunyawong N, et al. Osteoclast-derived apoptotic bodies show extended biological effects of parental cell in promoting bone defect healing. Theranostics, 2020, 10(15): 6825-6838.
35. Bai Y, Gong X, Dong R, et al. Long non-coding RNA HCAR promotes endochondral bone repair by upregulating VEGF and MMP13 in hypertrophic chondrocyte through sponging miR-15b-5p. Genes Dis, 2020, 9(2): 456-465.
36. Alshaer W, Zureigat H, Al Karaki A, et al. siRNA: Mechanism of action, challenges, and therapeutic approaches. Eur J Pharmacol, 2021, 905: 174178. doi: 10.1016/j.ejphar.2021.174178.
37. Leng Q, Chen L, Lv Y. RNA-based scaffolds for bone regeneration: application and mechanisms of mRNA, miRNA and siRNA. Theranostics, 2020, 10(7): 3190-3205.
38. Cui Y, Guo Y, Kong L, et al. A bone-targeted engineered exosome platform delivering siRNA to treat osteoporosis. Bioact Mater, 2021, 10: 207-221.
39. Liang S, Ling S, Du R, et al. The coupling of reduced type H vessels with unloading-induced bone loss and the protection role of Panax quinquefolium saponin in the male mice. Bone, 2021, 143: 115712. doi: 10.1016/j.bone.2020.115712.
40. Yang C, Liu Y, Wang Z, et al. Controlled mechanical loading improves bone regeneration by regulating type H vessels in a S1Pr1-dependent manner. FASEB J, 2022, 36(10): e22530. doi: 10.1096/fj.202200339RRR.
41. Huang J, Li YY, Xia K, et al. Harmine targets inhibitor of DNA binding-2 and activator protein-1 to promote preosteoclast PDGF-BB production. J Cell Mol Med, 2021, 25(12): 5525-5533.
42. Li Z, Xue H, Tan G, et al. Effects of miRNAs, lncRNAs and circRNAs on osteoporosis as regulatory factors of bone homeostasis (Review). Mol Med Rep, 2021, 24(5): 788. doi: 10.3892/mmr.2021.12428.
43. Wu W, Lu BF, Jiang RQ, et al. The function and regulation mechanism of piRNAs in human cancers. Histol Histopathol, 2021, 36(8): 807-816.
44. Hueso M, Mallén A, Suñé-Pou M, et al. ncRNAs in therapeutics: Challenges and limitations in nucleic acid-based drug delivery. Int J Mol Sci, 2021, 22(21): 11596. doi: 10.3390/ijms222111596.

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