The present research and progress of angiopoietin in diabetic retinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Liu Qingyan , Shao Yan ,  Li Xiaorong

Tianjin Key Laboratory of Retinal Functions and Diseases, Tianjin Branch of National Clinical Research Center for Ocular Disease, Eye Institute and School of Optometry, Tianjin Medical University Eye Hospital, Tianjin 300383, China;

Corresponding author：

Li Xiaorong, Email: xiaorli@163.com

Keywords：

Angiopoietins; Diabetic retinopathy; Receptor protein-tyrosine kinases; Lipid metabolism; Review

DOI：

10.3760/cma.j.cn511434-20210707-00364

Video：

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Abstract Full text Figures/Tables Video References Cited by

Diabetic retinopathy (DR) is one of the most common microvascular complications of diabetes, and it is the main cause of vision loss in diabetic patients. Angiopoietin (Ang), a superfamily of secreted proteins, is a vascular growth factor that regulates the stability of vascular environment, participates in angiogenesis and repair, and lipid metabolism. It plays an important role in the development of DR and has become a new target for the treatment of diabetic retinopathy. With the in-depth study of Ang and the research and development of various drugs for Ang, it is expected to bring new ideas and strategies for the treatment of DR in the future.

Citation： Liu Qingyan, Shao Yan, Li Xiaorong. The present research and progress of angiopoietin in diabetic retinopathy. Chinese Journal of Ocular Fundus Diseases, 2022, 38(11): 944-948. doi: 10.3760/cma.j.cn511434-20210707-00364 Copy

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4.	Morelli MB, Chavez C, Santulli G. Angiopoietin-like proteins as therapeutic targets for cardiovascular disease: focus on lipid disorders[J]. Expert Opin Ther Targets, 2020, 24(1): 79-88. DOI: 10.1080/14728222.2020.1707806.
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1. Matuszewski W, Baranowska-Jurkun A, Stefanowicz-Rutkowska MM, et al. The safety of pharmacological and surgical treatment of diabetes in patients with diabetic retinopathy-a review[J]. J Clin Med, 2021, 10(4): 705. DOI: 10.3390/jcm10040705.
2. Nicolini G, Forini F, Kusmic C, et al. Angiopoietin 2 signal complexity in cardiovascular disease and cancer[J/OL]. Life Sci, 2019, 239: 117080[2019-12-15]. https://pubmed.ncbi.nlm.nih.gov/31756341/. DOI: 10.1016/j.lfs.2019.117080.
3. Campochiaro PA, Peters KG. Targeting Tie2 for treatment of diabetic tetinopathy and diabetic macular edema[J]. Curr Diab Rep, 2016, 16(12): 126. DOI: 10.1007/s11892-016-0816-5.
4. Morelli MB, Chavez C, Santulli G. Angiopoietin-like proteins as therapeutic targets for cardiovascular disease: focus on lipid disorders[J]. Expert Opin Ther Targets, 2020, 24(1): 79-88. DOI: 10.1080/14728222.2020.1707806.
5. Ehrlich KC, Lacey M, Ehrlich M. Tissue-specific epigenetics of atherosclerosis-related ANGPT and ANGPTL genes[J]. Epigenomics, 2019, 11(2): 169-186. DOI: 10.2217/epi-2018-0150.
6. Bini S, D'Erasmo L, Di Costanzo A, et al. The interplay between angiopoietin-like proteins and adipose tissue: another piece of the relationship between adiposopathy and cardiometabolic diseases?[J]. Int J Mol Sci, 2021, 22(2): 742. DOI: 10.3390/ijms22020742.
7. Nguyen QD, Heier JS, Do DV, et al. The Tie2 signaling pathway in retinal vascular diseases: a novel therapeutic target in the eye[J]. Int J Retina Vitreous, 2020, 6: 48. DOI: 10.1186/s40942-020-00250-z.
8. Saharinen P, Eklund L, Alitalo K. Therapeutic targeting of the angiopoietin-TIE pathway[J]. Nat Rev Drug Discov, 2017, 16(9): 635-661. DOI: 10.1038/nrd.2016.278.
9. Joussen AM, Ricci F, Paris LP, et al. Angiopoietin/Tie2 signalling and its role in retinal and choroidal vascular diseases: a review of preclinical data[J]. Eye (Lond), 2021, 35(5): 1305-1316. DOI: 10.1038/s41433-020-01377-x.
10. Tee JK, Setyawati MI, Peng F, et al. Angiopoietin-1 accelerates restoration of endothelial cell barrier integrity from nanoparticleinduced leakiness[J]. Nanotoxicology, 2019, 13(5): 682-700. DOI: 10.1080/17435390.2019.1571646.
11. Yun JH, Han MH, Jeong HS, et al. Angiopoietin 1 attenuates interleukin-6-induced endothelial cell permeability through SHP-1[J]. Biochem Biophys Res Commun, 2019, 518(2): 286-293. DOI: 10.1016/j.bbrc.2019.08.048.
12. Cheema MR, DaCosta J, Talks J, et al. Ten-year real-world outcomes of anti-vascular endothelial growth factor therapy in neovascular age-related macular degeneration[J]. Clin Ophthalmol, 2021, 15: 279-287. DOI: 10.2147/OPTH.S269162.
13. Lee J, Park DY, Park DY, et al. Angiopoietin-1 suppresses choroidal neovascularization and vascular leakage[J]. Invest Ophthalmol Vis Sci, 2014, 55(4): 2191-2199. DOI: 10.1167/iovs.14-13897.
14. Rochfort KD, Carroll LS, Barabas P, et al. COMP-ang1 stabilizes hyperglycemic disruption of blood-retinal barrier phenotype in human retinal microvascular endothelial cells[J]. Invest Ophthalmol Vis Sci, 2019, 60(10): 3547-3555. DOI: 10.1167/iovs.19-27644.
15. Cahoon JM, Rai RR, Carroll LS, et al. Intravitreal AAV2. COMP-ang1 prevents neurovascular degeneration in a murine model of diabetic retinopathy[J]. Diabetes, 2015, 64(12): 4247-4259. DOI: 10.2337/db14-1030.
16. Park SW, Yun JH, Kim JH, et al. Angiopoietin 2 induces pericyte apoptosis via Alpha3beta1 integrin signaling in diabetic retinopathy[J]. Diabetes, 2014, 63(9): 3057-3068. DOI: 10.2337/db13-1942.
17. Menden H, Welak S, Cossette S, et al. Lipopolysaccharide (LPS)-mediated angiopoietin-2-dependent autocrine angiogenesis is regulated by nadph oxidase 2 (Nox2) in human pulmonary microvascular endothelial cells[J]. J Biol Chem, 2015, 290(9): 5449-5461. DOI: 10.1074/jbc.M114.600692.
18. Whitehead M, Osborne A, Widdowson PS, et al. Angiopoietins in diabetic retinopathy: current understanding and therapeutic potential[J/OL]. Diabetes Res, 2019, 2019: 5140521[2019-08-14]. https://pubmed.ncbi.nlm.nih.gov/31485452/. DOI: 10.1155/2019/5140521.
19. Park DY, Lee J, Kim J, et al. Plastic roles of pericytes in the blood-retinal barrier[J/OL]. Nat Commun, 2017, 8: 15296[2017-05-16]. https://pubmed.ncbi.nlm.nih.gov/28508859/. DOI: 10.1038/ncomms15296.
20. Chatterjee A, Eshwaran R, Huang H, et al. Role of the Ang2-Tie2 axis in vascular damage driven by high glucose or nucleoside diphosphate kinase B deficiency[J/OL]. Int J Mol Sci, 2020, 21(10): 3713[2020-05-25]. https://pubmed.ncbi.nlm.nih.gov/32466219/. DOI: 10.3390/ijms21103713.
21. Khalaf N, Helmy H, Labib H, et al. Role of Angiopoietins and Tie-2 in diabetic retinopathy[J]. Electron Physician, 2017, 9(8): 5031-5035. DOI: 10.19082/5031.
22. Keles A, Sonmez K, Erol YO, et al. Vitreous levels of vascular endothelial growth factor, stromal cell-derived factor-1α, and angiopoietin-like protein 2 in patients with active proliferative diabetic retinopathy[J]. Graefe's Arch Clin Exp Ophthalmol, 2021, 259(1): 53-60. DOI: 10.1007/s00417-020-04889-0.
23. Yin R, Zhang N, Zhang D, et al. Higher levels of circulating ANGPTL2 are associated with macular edema in patients with type 2 diabetes[J/OL]. Medicine (Baltimore), 2021, 100(6): e24638[2021-02-12]. https://pubmed.ncbi.nlm.nih.gov/33578584/. DOI: 10.1097/MD.0000000000024638.
24. Hussain RM, Neiweem AE, Kansara V, et al. Tie-2/Angiopoietin pathway modulation as a therapeutic strategy for retinal disease[J]. Expert Opin Investig Drugs, 2019, 28(10): 861-869. DOI: 10.1080/13543784.2019.1667333.
25. 邵彦, 李筱荣. 从能量代谢角度看糖尿病相关眼病的诊疗[J]. 中华实验眼科杂志, 2020, 38(9): 729-732. DOI: 10.3760/cma.j.cn115989-20200527-00377.Shao Y, Li XR. A metabolic perspective in diabetic ocular disease[J]. Chin J Exp Ophthalmol, 2020, 38(9): 729-732. DOI: 10.3760/cma.j.cn115989-20200527-00377.
26. Jin N, Matter WF, Michael LF, et al. The Angiopoietin-like protein 3 and 8 complex interacts with lipoprotein lipase and induces LPL cleavage[J]. ACS Chem Biol, 2021, 16(3): 457-462. DOI: 10.1021/acschembio.0c00954.
27. Gunn KH, Gutgsell AR, Xu Y, et al. Comparison of angiopoietin-like protein 3 and 4 reveals structural and mechanistic similarities[J/OL]. Biol Chem, 2021, 296: 100312[2021-01-20]. https://pubmed.ncbi.nlm.nih.gov/33482195/. DOI: 10.1016/j.jbc.2021.100312.
28. Gomez Perdiguero E, Liabotis-Fontugne A, Durand M, et al. ANGPTL4-αvβ3 interaction counteracts hypoxia-induced vascular permeability by modulating Src signalling downstream of vascular endothelial growth factor receptor 2[J]. J Pathol, 2016, 240(4): 461-471. DOI: 10.1002/path.4805.
29. Yu CG, Yuan SS, Yang LY, et al. Angiopoietin-like 3 is a potential biomarker for retinopathy in type 2 diabetic patients[J]. Am J Ophthalmol, 2018, 191: 34-41. DOI: 10.1016/j.ajo.2018.03.040.
30. Gaudet D, Karwatowska-Prokopczuk E, Baum SJ, et al. Vupanorsen, an N-acetyl galactosamine-conjugated antisense drug to ANGPTL3 mRNA, lowers triglycerides and atherogenic lipoproteins in patients with diabetes, hepatic steatosis, and hypertriglyceridaemia[J]. Eur Heart J, 2020, 41(40): 3936-3945. DOI: 10.1093/eurheartj/ehaa689.
31. Yang LY, Yu CG, Wang XH, et al. Angiopoietin-like protein 4 is a high-density lipoprotein (HDL) component for HDL metabolism and function in nondiabetic participants and type-2 diabetic patients[J/OL]. Am Heart Assoc, 2017, 6(6): e005973[2017-06-23]. https://pubmed.ncbi.nlm.nih.gov/28645936/. DOI: 10.1161/JAHA.117.005973.
32. Leth-Espensen KZ, Kristensen KK, Kumari A, et al. The intrinsic instability of the hydrolase domain of lipoprotein lipase facilitates its inactivation by ANGPTL4-catalyzed[J/OL]. Proc Natl Acad Sci USA, 2021, 118(12): e2026650118[2021-03-23]. https://pubmed.ncbi.nlm.nih.gov/33723082/. DOI: 10.1073/pnas.2026650118.
33. Barchetta I, Chiappetta C, Ceccarelli V, et al. Angiopoietin-like protein 4 overexpression in visceral adipose tissue from obese subjects with impaired glucose metabolism and relationship with lipoprotein lipase[J/OL]. Int J Mol Sci, 2020, 21(19): 7197[2020-09-29]. https://pubmed.ncbi.nlm.nih.gov/33003532/. DOI: 10.3390/ijms21197197.
34. Babapoor-Farrokhran S, Jee K, Puchner B, et al. Angiopoietin-like 4 is a potent angiogenic factor and a novel therapeutic target for patients with proliferative diabetic retinopathy[J/OL]. Proc Natl Acad Sci USA, 2015, 112(23): E3030-3039[2015-06-09]. https://pubmed.ncbi.nlm.nih.gov/26039997/. DOI: 10.1073/pnas.1423765112.
35. Lu Q, Zou W, Chen B, et al. ANGPTL-4 correlates with vascular endothelial growth factor in patients with proliferative diabetic retinopathy[J]. Graefe's Arch Clin Exp Ophthalmol, 2016, 254(7): 1281-1288. DOI: 10.1007/s00417-015-3187-8.
36. Yang X, Cao J, Du Y, et al. Angiopoietin-like protein 4 (ANGPTL4) induces retinal pigment epithelial barrier breakdown by activating signal transducer and activator of transcription 3 (STAT3): evidence from ARPE-19 cells under hypoxic condition and diabetic rats[J]. Med Sci Monit, 2019, 25: 6742-6754. DOI: 10.12659/MSM.915748.
37. Surma S, Romańczyk M, Filipiak KJ. Angiopoietin-like proteins inhibitors: new horizons in the treatment of atherogenic dyslipidemia and familial hypercholesterolemia[J]. Cardiol J, 2021, 2021: E1(2021-07-07)[2021-01-20]. https://pubmed.ncbi.nlm.nih.gov/33470417/. DOI: 10.5603/CJ.a2021.0006. [published online ahead of print].
38. Siddiqa A, Cirillo E, Tareen SHK, et al. Visualizing the regulatory role of angiopoietin-like protein 8 (ANGPTL8) in glucose and lipid metabolic pathways[J]. Genomics, 2017, 109(5-6): 408-418. DOI: 10.1016/j.ygeno.2017.06.006.
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