Advances in the effect of neurovascular unit in retinal physiological and pathological process_Chinese Journal of Ocular Fundus Diseases

Authors：

Huang Xinyuan , Shao Yan ,  Li Xiaorong

Tianjin Key Laboratory of Retinal Functions and Diseases, Tianjin International Joint Research and Development Centre of Ophthalmology and Vision Science, Eye Institute and School of Optometry, Tianjin Medical University Eye Hospital, Tianjin 300384, China;
Huang Xinyuan and Shao Yan are contributed equally to the article;

Corresponding author：

Li Xiaorong, Email: xiaorli@163.com

Keywords：

Retinal diseases; Review; Neurovascular unit

DOI：

10.3760/cma.j.cn511434-20210111-00013

Video：

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Neurovascular unit (NVU) refers to a functional complex of neural cells and vasculature, which plays an important role in maintaining retinal homeostasis and matching metabolic demands. In physiological situation, retinal NVU mainly exerts two effects: (1) maintaining blood-retinal barrier for retinal homeostasis maintenance; (2) regulating local blood flow to meet metabolic and functional demands of the retina. The pathological changes in retinal diseases are reflected in each functional part of retinal NVU, including cell-cell connections, signal pathways, metabolic activities and cellular functions. However, the main pattern and manifestation of NVU impairment differs among retinal diseases due to different etiologies. At present, understanding on retinal NVU is still insufficient, and its clinical application is even more limited. Further application in the diagnosis and treatment of retinal diseases is an important direction for future research on NVU.

Citation： Huang Xinyuan, Shao Yan, Li Xiaorong. Advances in the effect of neurovascular unit in retinal physiological and pathological process. Chinese Journal of Ocular Fundus Diseases, 2022, 38(2): 168-172. doi: 10.3760/cma.j.cn511434-20210111-00013 Copy

1.	Muoio V, Persson PB, Sendeski MM. The neurovascular unit-concept review[J]. Acta Physiologica, 2014, 210(4): 790-798. DOI: 10.1111/apha.12250.
2.	Newman EA. Functional hyperemia and mechanisms of neurovascular coupling in the retinal vasculature[J]. J Cerebr Blood F Met, 2013, 33(11): 1685-1695. DOI: 10.1038/jcbfm.2013.145.
3.	Simó R, Stitt AW, Gardner TW. Neurodegeneration in diabetic retinopathy: does it really matter?[J]. Diabetologia, 2018, 61(9): 1902-1912. DOI: 10.1007/s00125-018-4692-1.
4.	van der Wijk A, Vogels IMC, van Veen HA, et al. Spatial and temporal recruitment of the neurovascular unit during development of the mouse blood-retinal barrier[J]. Tissue Cell, 2018, 52: 42-50. DOI: 10.1016/j.tice.2018.03.010.
5.	Biswas S, Cottarelli A, Agalliu D. Neuronal and glial regulation of CNS angiogenesis and barriergenesis[J/OL]. Development, 2020, 147(9): dev182279[2020-05-01]. https://pubmed.ncbi.nlm.nihgov/32358096/. DOI: 10.1242/dev.182279.
6.	Rathnasamy G, Foulds WS, Ling EA, et al. Retinal microglia-a key player in healthy and diseased retina[J]. Prog Neurobiol, 2019, 173: 18-40. DOI: 10.1016/j.pneurobio.2018.05.006.
7.	Jing C, Liu CH, Sapieha P. Retinal vascular development[M]//Stahl A. Anti-angiogenic therapy in ophthalmology. Cham: Springer, 2016: 1-19.
8.	García-Ayuso D, Di Pierdomenico J, Vidal-Sanz M, et al. Retinal ganglion cell death as a late remodeling effect of photoreceptor degeneration[J/OL]. Int J Mol Sci, 2019, 20(18): 4649[2019-09-19]. https://pubmed.ncbi.nlm.nih.gov/31546829/. DOI: 10.3390/ijms20184649.
9.	Telias M, Nawy S, Kramer RH. Degeneration-dependent retinal remodeling: looking for the molecular trigger[J/OL]. Front Neurosci, 2020, 14: 618019[2020-12-18]. https://pubmed.ncbi.nlm.nih.gov/33390897/. DOI: 10.3389/fnins.2020.618019.
10.	Zihni C, Mills C, Matter K, et al. Tight junctions: from simple barriers to multifunctional molecular gates[J]. Nat Rev Mol Cell Biol, 2016, 17(9): 564-580. DOI: 10.1038/nrm.2016.80.
11.	Trost A, Bruckner D, Rivera FJ, et al. Pericytes in the retina[J]. Adv Exp Med Biol, 2019, 1122: 1-26. DOI: 10.1007/978-3-030-11093-2_1.
12.	Newman EA. Glial cell regulation of neuronal activity and blood flow in the retina by release of gliotransmitters[J/OL]. Philos Trans R Soc Lond B Biol Sci, 2015, 370(1672): 20140195[2015-07-05]. https://pubmed.ncbi.nlm.nih.gov/26009774/. DOI: 10.1098/rstb.2014.0195.
13.	Nakagawa S, Deli MA, Nakao S, et al. Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells[J]. Cell Mol Neurobiol, 2007, 27(6): 687-694. DOI: 10.1007/s10571-007-9195-4.
14.	Eleftheriou CG, Ivanova E, Sagdullaev BT. Of neurons and pericytes: the neuro-vascular approach to diabetic retinopathy[J/OL]. Visual Neurosci, 2020, 37: E005[2020-08-11]. https://pubmed.ncbi.nlm.nih.gov/32778188/. DOI: 10.1017/S0952523820000048.
15.	Someya E, Akagawa M, Mori A, et al. Role of neuron-glia signaling in regulation of retinal vascular tone in rats[J/OL]. Int J Mol Sci, 2019, 20(8): 1952[2019-04-20]. https://pubmed.ncbi.nlm.nih.gov/31010057/. DOI: 10.3390/ijms20081952.
16.	Kur J, Newman EA, Chan-Ling T. Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease[J]. Prog Retin Eye Res, 2012, 31(5): 377-406. DOI: 10.1016/j.preteyeres.2012.04.004.
17.	Hein TW, Yuan Z, Rosa RH, et al. Requisite roles of A2A receptors, nitric oxide, and KATP channels in retinal arteriolar dilation in response to adenosine[J/OL]. Invest Ophthalmol Vis Sci, 2005, 46(6): 2113[2005-05-01]. https://pubmed.ncbi.nlm.nih.gov/15914631/. DOI: 10.1167/iovs.04-1438.
18.	Biesecker KR, Srienc AI, Shimoda AM, et al. Glial cell calcium signaling mediates capillary regulation of blood flow in the retina[J]. J Neurosci, 2016, 36(36): 9435-9445. DOI: 10.1523/JNEUROSCI.1782-16.
19.	Phipps JA, Dixon MA, Jobling AI, et al. The renin-angiotensin system and the retinal neurovascular unit: a role in vascular regulation and disease[J/OL]. Exp Eye Res, 2019, 187: 107753[2019-08-10]. https://pubmed.ncbi.nlm.nih.gov/31408629/. DOI: 10.1016/j.exer.2019.107753.
20.	Friedrichs P, Schlotterer A, Sticht C, et al. Hyperglycaemic memory affects the neurovascular unit of the retina in a diabetic mouse model[J]. Diabetologia, 2017, 60(7): 1354-1358. DOI: 10.1007/s00125-017-4254-y.
21.	Lajko M, Cardona HJ, Taylor JM, et al. Hyperoxia-induced proliferative retinopathy: early interruption of retinal vascular development with severe and irreversible neurovascular disruption[J/OL]. PLoS One, 2016, 11(11): e166886[2016-11-18]. https://pubmed.ncbi.nlm.nih.gov/27861592/. DOI: 10.1371/journal.pone.0166886.
22.	Mohamed IN, Ishrat T, Fagan SC, et al. Role of inflammasome activation in the pathophysiology of vascular diseases of the neurovascular unit[J]. Antioxid Redox Sign, 2015, 22(13): 1188-1206. DOI: 10.1089/ars.2014.6126.
23.	Sinclair SH, Schwartz SS. Diabetic retinopathy-an underdiagnosed and undertreated inflammatory, neuro-vascular complication of diabetes[J/OL]. Front Endocrinol (Lausanne), 2019, 10: 843[2019-12-13]. https://pubmed.ncbi.nlm.nih.gov/31920963/. DOI: 10.3389/fendo.2019.00843.
24.	García-Ayuso D, Salinas-Navarro M, Agudo M, et al. Retinal ganglion cell numbers and delayed retinal ganglion cell death in the P23H rat retina[J]. Exp Eye Res, 2010, 91(6): 800-810. DOI: 10.1016/j.exer.2010.10.003.
25.	García-Ayuso D, Salinas-Navarro M, Nadal-Nicolás FM, et al. Sectorial loss of retinal ganglion cells in inherited photoreceptor degeneration is due to RGC death[J]. Brit J Ophthalmol, 2014, 98(3): 396-401. DOI: 10.1136/bjophthalmol-2013-303958.
26.	Yang S, Zhang J, Chen L. The cells involved in the pathological process of diabetic retinopathy[J/OL]. Biomed Pharmacother, 2020, 132: 110818[2020-10-11].https://pubmed.ncbi.nlm.nih.gov/33053509/. DOI: 10.1016/j.biopha.2020.110818.
27.	Gastinger MJ, Singh RS, Barber AJ. Loss of cholinergic and dopaminergic amacrine cells in streptozotocin-diabetic rat and Ins2Akita-diabetic mouse retinas[J]. Invest Ophthalmol Vis Sci, 2006, 47(7): 3143-3150. DOI: 10.1167/iovs.05-1376.
28.	Cuenca N, Fernández-Sánchez L, Campello L, et al. Cellular responses following retinal injuries and therapeutic approaches for neurodegenerative diseases[J]. Prog Retin Eye Res, 2014, 43: 17-75. DOI: 10.1016/j.preteyeres.2014.07.001.
29.	Gugleta K, Kochkorov A, Waldmann N, et al. Dynamics of retinal vessel response to flicker light in glaucoma patients and ocular hypertensives[J]. Graefe's Arch Clin Exp Ophthalmol, 2012, 250(4): 589-594. DOI: 10.1007/s00417-011-1842-2.
30.	Wareham LK, Calkins DJ. The neurovascular unit in glaucomatous neurodegeneration[J/OL]. Front Cell Dev Biol, 2020, 8: 452[2020-06-16]. https://pubmed.ncbi.nlm.nih.gov/32656207/. DOI: 10.3389/fcell.2020.00452.
31.	Syc-Mazurek SB, Libby RT. Axon injury signaling and compartmentalized injury response in glaucoma[J/OL]. Prog Retin Eye Res, 2019, 73: 100769[2019-07-10]. https://pubmed.ncbi.nlm.nih.gov/31301400/. DOI: 10.1016/j.preteyeres.2019.07.002.
32.	Kerr NM, Johnson CS, Zhang J, et al. High pressure-induced retinal ischaemia reperfusion causes upregulation of gap junction protein connexin43 prior to retinal ganglion cell loss[J]. Exp Neurol, 2012, 234(1): 144-152. DOI: 10.1016/j.expneurol.2011.12.027.
33.	Handa JT, Bowes Rickman C, Dick AD, et al. A systems biology approach towards understanding and treating non-neovascular age-related macular degeneration[J/OL]. Nat Commun, 2019, 10(1): 3347[2019-07-26]. https://pubmed.ncbi.nlm.nih.gov/31350409/. DOI: 10.1038/s41467-019-11262-1.
34.	Burgansky-Eliash Z, Barash H, Nelson D, et al. Retinal blood flow velocity in patients with age-related macular degeneration[J]. Curr Eye Res, 2013, 39(3): 304-311. DOI: 10.3109/02713683.2013.840384.
35.	Lanzl IM, Seidova S, Maier M, et al. Dynamic retinal vessel response to flicker in age-related macular degeneration patients before and after vascular endothelial growth factor inhibitor injection[J]. Acta Ophthalmol, 2011, 89(5): 472-479. DOI: 10.1111/j.1755-3768.2009.01718.x.
36.	Hudson N, Cahill M, Campbell M. Inner blood-retina barrier involvement in dry age-related macular degeneration (AMD) pathology[J]. Neural Regen Res, 2020, 15(9): 1656-1657. DOI: 10.4103/1673-5374.276332.
37.	Lim LS, Ling LH, Ong PG, et al. Dynamic responses in retinal vessel caliber with flicker light stimulation and risk of diabetic retinopathy and its progression[J]. Invest Ophthalmol Vis Sci, 2017, 58(5): 2449-2455. DOI: 10.1167/iovs.16-21008.
38.	Kim SR, Suh W. Beneficial effects of the Src inhibitor, dasatinib, on breakdown of the blood-retinal barrier[J]. Arch Pharm Res, 2017, 40(2): 197-203. DOI: 10.1007/s12272-016-0872-z.
39.	Di Pierdomenico J, Scholz R, Valiente-Soriano FJ, et al. Neuroprotective effects of FGF2 and minocycline in two animal models of inherited retinal degeneration[J]. Invest Ophthalmol Vis Sci, 2018, 59(11): 4392-4403. DOI: 10.1167/iovs.18-24621.

1. Muoio V, Persson PB, Sendeski MM. The neurovascular unit-concept review[J]. Acta Physiologica, 2014, 210(4): 790-798. DOI: 10.1111/apha.12250.
2. Newman EA. Functional hyperemia and mechanisms of neurovascular coupling in the retinal vasculature[J]. J Cerebr Blood F Met, 2013, 33(11): 1685-1695. DOI: 10.1038/jcbfm.2013.145.
3. Simó R, Stitt AW, Gardner TW. Neurodegeneration in diabetic retinopathy: does it really matter?[J]. Diabetologia, 2018, 61(9): 1902-1912. DOI: 10.1007/s00125-018-4692-1.
4. van der Wijk A, Vogels IMC, van Veen HA, et al. Spatial and temporal recruitment of the neurovascular unit during development of the mouse blood-retinal barrier[J]. Tissue Cell, 2018, 52: 42-50. DOI: 10.1016/j.tice.2018.03.010.
5. Biswas S, Cottarelli A, Agalliu D. Neuronal and glial regulation of CNS angiogenesis and barriergenesis[J/OL]. Development, 2020, 147(9): dev182279[2020-05-01]. https://pubmed.ncbi.nlm.nihgov/32358096/. DOI: 10.1242/dev.182279.
6. Rathnasamy G, Foulds WS, Ling EA, et al. Retinal microglia-a key player in healthy and diseased retina[J]. Prog Neurobiol, 2019, 173: 18-40. DOI: 10.1016/j.pneurobio.2018.05.006.
7. Jing C, Liu CH, Sapieha P. Retinal vascular development[M]//Stahl A. Anti-angiogenic therapy in ophthalmology. Cham: Springer, 2016: 1-19.
8. García-Ayuso D, Di Pierdomenico J, Vidal-Sanz M, et al. Retinal ganglion cell death as a late remodeling effect of photoreceptor degeneration[J/OL]. Int J Mol Sci, 2019, 20(18): 4649[2019-09-19]. https://pubmed.ncbi.nlm.nih.gov/31546829/. DOI: 10.3390/ijms20184649.
9. Telias M, Nawy S, Kramer RH. Degeneration-dependent retinal remodeling: looking for the molecular trigger[J/OL]. Front Neurosci, 2020, 14: 618019[2020-12-18]. https://pubmed.ncbi.nlm.nih.gov/33390897/. DOI: 10.3389/fnins.2020.618019.
10. Zihni C, Mills C, Matter K, et al. Tight junctions: from simple barriers to multifunctional molecular gates[J]. Nat Rev Mol Cell Biol, 2016, 17(9): 564-580. DOI: 10.1038/nrm.2016.80.
11. Trost A, Bruckner D, Rivera FJ, et al. Pericytes in the retina[J]. Adv Exp Med Biol, 2019, 1122: 1-26. DOI: 10.1007/978-3-030-11093-2_1.
12. Newman EA. Glial cell regulation of neuronal activity and blood flow in the retina by release of gliotransmitters[J/OL]. Philos Trans R Soc Lond B Biol Sci, 2015, 370(1672): 20140195[2015-07-05]. https://pubmed.ncbi.nlm.nih.gov/26009774/. DOI: 10.1098/rstb.2014.0195.
13. Nakagawa S, Deli MA, Nakao S, et al. Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells[J]. Cell Mol Neurobiol, 2007, 27(6): 687-694. DOI: 10.1007/s10571-007-9195-4.
14. Eleftheriou CG, Ivanova E, Sagdullaev BT. Of neurons and pericytes: the neuro-vascular approach to diabetic retinopathy[J/OL]. Visual Neurosci, 2020, 37: E005[2020-08-11]. https://pubmed.ncbi.nlm.nih.gov/32778188/. DOI: 10.1017/S0952523820000048.
15. Someya E, Akagawa M, Mori A, et al. Role of neuron-glia signaling in regulation of retinal vascular tone in rats[J/OL]. Int J Mol Sci, 2019, 20(8): 1952[2019-04-20]. https://pubmed.ncbi.nlm.nih.gov/31010057/. DOI: 10.3390/ijms20081952.
16. Kur J, Newman EA, Chan-Ling T. Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease[J]. Prog Retin Eye Res, 2012, 31(5): 377-406. DOI: 10.1016/j.preteyeres.2012.04.004.
17. Hein TW, Yuan Z, Rosa RH, et al. Requisite roles of A2A receptors, nitric oxide, and KATP channels in retinal arteriolar dilation in response to adenosine[J/OL]. Invest Ophthalmol Vis Sci, 2005, 46(6): 2113[2005-05-01]. https://pubmed.ncbi.nlm.nih.gov/15914631/. DOI: 10.1167/iovs.04-1438.
18. Biesecker KR, Srienc AI, Shimoda AM, et al. Glial cell calcium signaling mediates capillary regulation of blood flow in the retina[J]. J Neurosci, 2016, 36(36): 9435-9445. DOI: 10.1523/JNEUROSCI.1782-16.
19. Phipps JA, Dixon MA, Jobling AI, et al. The renin-angiotensin system and the retinal neurovascular unit: a role in vascular regulation and disease[J/OL]. Exp Eye Res, 2019, 187: 107753[2019-08-10]. https://pubmed.ncbi.nlm.nih.gov/31408629/. DOI: 10.1016/j.exer.2019.107753.
20. Friedrichs P, Schlotterer A, Sticht C, et al. Hyperglycaemic memory affects the neurovascular unit of the retina in a diabetic mouse model[J]. Diabetologia, 2017, 60(7): 1354-1358. DOI: 10.1007/s00125-017-4254-y.
21. Lajko M, Cardona HJ, Taylor JM, et al. Hyperoxia-induced proliferative retinopathy: early interruption of retinal vascular development with severe and irreversible neurovascular disruption[J/OL]. PLoS One, 2016, 11(11): e166886[2016-11-18]. https://pubmed.ncbi.nlm.nih.gov/27861592/. DOI: 10.1371/journal.pone.0166886.
22. Mohamed IN, Ishrat T, Fagan SC, et al. Role of inflammasome activation in the pathophysiology of vascular diseases of the neurovascular unit[J]. Antioxid Redox Sign, 2015, 22(13): 1188-1206. DOI: 10.1089/ars.2014.6126.
23. Sinclair SH, Schwartz SS. Diabetic retinopathy-an underdiagnosed and undertreated inflammatory, neuro-vascular complication of diabetes[J/OL]. Front Endocrinol (Lausanne), 2019, 10: 843[2019-12-13]. https://pubmed.ncbi.nlm.nih.gov/31920963/. DOI: 10.3389/fendo.2019.00843.
24. García-Ayuso D, Salinas-Navarro M, Agudo M, et al. Retinal ganglion cell numbers and delayed retinal ganglion cell death in the P23H rat retina[J]. Exp Eye Res, 2010, 91(6): 800-810. DOI: 10.1016/j.exer.2010.10.003.
25. García-Ayuso D, Salinas-Navarro M, Nadal-Nicolás FM, et al. Sectorial loss of retinal ganglion cells in inherited photoreceptor degeneration is due to RGC death[J]. Brit J Ophthalmol, 2014, 98(3): 396-401. DOI: 10.1136/bjophthalmol-2013-303958.
26. Yang S, Zhang J, Chen L. The cells involved in the pathological process of diabetic retinopathy[J/OL]. Biomed Pharmacother, 2020, 132: 110818[2020-10-11].https://pubmed.ncbi.nlm.nih.gov/33053509/. DOI: 10.1016/j.biopha.2020.110818.
27. Gastinger MJ, Singh RS, Barber AJ. Loss of cholinergic and dopaminergic amacrine cells in streptozotocin-diabetic rat and Ins2Akita-diabetic mouse retinas[J]. Invest Ophthalmol Vis Sci, 2006, 47(7): 3143-3150. DOI: 10.1167/iovs.05-1376.
28. Cuenca N, Fernández-Sánchez L, Campello L, et al. Cellular responses following retinal injuries and therapeutic approaches for neurodegenerative diseases[J]. Prog Retin Eye Res, 2014, 43: 17-75. DOI: 10.1016/j.preteyeres.2014.07.001.
29. Gugleta K, Kochkorov A, Waldmann N, et al. Dynamics of retinal vessel response to flicker light in glaucoma patients and ocular hypertensives[J]. Graefe's Arch Clin Exp Ophthalmol, 2012, 250(4): 589-594. DOI: 10.1007/s00417-011-1842-2.
30. Wareham LK, Calkins DJ. The neurovascular unit in glaucomatous neurodegeneration[J/OL]. Front Cell Dev Biol, 2020, 8: 452[2020-06-16]. https://pubmed.ncbi.nlm.nih.gov/32656207/. DOI: 10.3389/fcell.2020.00452.
31. Syc-Mazurek SB, Libby RT. Axon injury signaling and compartmentalized injury response in glaucoma[J/OL]. Prog Retin Eye Res, 2019, 73: 100769[2019-07-10]. https://pubmed.ncbi.nlm.nih.gov/31301400/. DOI: 10.1016/j.preteyeres.2019.07.002.
32. Kerr NM, Johnson CS, Zhang J, et al. High pressure-induced retinal ischaemia reperfusion causes upregulation of gap junction protein connexin43 prior to retinal ganglion cell loss[J]. Exp Neurol, 2012, 234(1): 144-152. DOI: 10.1016/j.expneurol.2011.12.027.
33. Handa JT, Bowes Rickman C, Dick AD, et al. A systems biology approach towards understanding and treating non-neovascular age-related macular degeneration[J/OL]. Nat Commun, 2019, 10(1): 3347[2019-07-26]. https://pubmed.ncbi.nlm.nih.gov/31350409/. DOI: 10.1038/s41467-019-11262-1.
34. Burgansky-Eliash Z, Barash H, Nelson D, et al. Retinal blood flow velocity in patients with age-related macular degeneration[J]. Curr Eye Res, 2013, 39(3): 304-311. DOI: 10.3109/02713683.2013.840384.
35. Lanzl IM, Seidova S, Maier M, et al. Dynamic retinal vessel response to flicker in age-related macular degeneration patients before and after vascular endothelial growth factor inhibitor injection[J]. Acta Ophthalmol, 2011, 89(5): 472-479. DOI: 10.1111/j.1755-3768.2009.01718.x.
36. Hudson N, Cahill M, Campbell M. Inner blood-retina barrier involvement in dry age-related macular degeneration (AMD) pathology[J]. Neural Regen Res, 2020, 15(9): 1656-1657. DOI: 10.4103/1673-5374.276332.
37. Lim LS, Ling LH, Ong PG, et al. Dynamic responses in retinal vessel caliber with flicker light stimulation and risk of diabetic retinopathy and its progression[J]. Invest Ophthalmol Vis Sci, 2017, 58(5): 2449-2455. DOI: 10.1167/iovs.16-21008.
38. Kim SR, Suh W. Beneficial effects of the Src inhibitor, dasatinib, on breakdown of the blood-retinal barrier[J]. Arch Pharm Res, 2017, 40(2): 197-203. DOI: 10.1007/s12272-016-0872-z.
39. Di Pierdomenico J, Scholz R, Valiente-Soriano FJ, et al. Neuroprotective effects of FGF2 and minocycline in two animal models of inherited retinal degeneration[J]. Invest Ophthalmol Vis Sci, 2018, 59(11): 4392-4403. DOI: 10.1167/iovs.18-24621.

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