Research status of nicotine-aggravating the choroidal neovascularization formation in wet age-related macular degeneration_Chinese Journal of Ocular Fundus Diseases

Authors：

Gong Yajun , Lai Kunbei ,  Jin Chenjin

State Key Laboratory of Ophthalmology, Zhongshan Ophthalmic Center, Sun Yat-sen University, Guangzhou 510060, China;

Corresponding author：

Jin Chenjin, Email: jinchj@mail.sysu.edu.cn

Keywords：

Wet macular degeneration/etiology; Choroidal neovascularization/etiology; Nicotine; Review

DOI：

10.3760/cma.j.cn511434-20180704-00226

Video：

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Choroidal neovascularization is the leading causes of central vision loss in wet age-related macular degeneration (wAMD) patients. Smoking not only aggravates the incidence and severity of the choroidal neovascularization of wAMD, but also affects the clinical treatment, making the prognosis worse. Nicotine, as an important harmful substance in tobacco, is an easily addictive and highly toxic alkaloid. Animal experiments and clinical studies have confirmed that nicotine can aggravate wAMD by mediating angiogenesis through nicotinic acetylcholine receptor, bone marrow blasts, inflammation, complement system, etc. Therefore, in order to early take appropriate intervention measures to prevent and delay the development, we should actively explore the exact pathogenesis by which nicotine aggravates the choroidal neovascularization.

Citation： Gong Yajun, Lai Kunbei, Jin Chenjin. Research status of nicotine-aggravating the choroidal neovascularization formation in wet age-related macular degeneration. Chinese Journal of Ocular Fundus Diseases, 2020, 36(4): 319-322. doi: 10.3760/cma.j.cn511434-20180704-00226 Copy

1.	Lim LS, Mitch P, Seddon JM, et al. Age-related macular degeneration[J]. Lancet, 2012, 379(9827): 1728-1738. DOI: 10.1016/S0140-6736(12)60282-7.
2.	Shao J, Choudhary MM, Schachat AP, et al. Neovascular age-related macular degeneration[J]. Dev Ophthalmol, 2016, 55: 125-136. DOI: 10.1159/000438969.
3.	Velilla S, Garcia-Medina JJ, Garcia-Layana A, et al. Smoking and age-related macular degeneration: review and update[J/OL]. J Ophthalmol, 2013, 2013: 895147[2013-12-04]. https://dx.doi.org/10.1155/2013/895147. DOI: 10.1155/2013/895147.
4.	Moracco KE, Morgan JC, Mendel J, et al. "My first thought was croutons": perceptions of cigarettes and cigarette smoke constituents among adult smokers and nonsmokers[J]. Nicotine Tob Res, 2015, 18(7): 1566-1574. DOI: 10.1093/ntr/ntv281.
5.	Willeford KT, Rapp J. Smoking and age-related macular degeneration: biochemical mechanisms and patient support[J]. Optom Vis Sci, 2012, 89(11): 1662-1666. DOI: 10.1097/OPX.0b013e31826c5df2.
6.	Suner IJ, Hernandez EP, Espinosaheidmann DG, et al. Nicotine increases size and severity of experimental choroidal neovascularization[J]. Invest Ophthalmol Vis Sci, 2004, 45(1): 311-317. DOI: 10.1167/iovs.03-0733.
7.	Lechanteur YT, VandeCamp PL, Smailhodzic D, et al. Association of smoking and CFH and ARMS2 risk variants with younger age at onset of neovascular age-related macular degeneration[J]. JAMA Ophthalmol, 2015, 133(5): 533-541. DOI: 10.1001/jamaophthalmol.2015.18.
8.	Vingerling JR, Hofman A, Grobbee DE, et al. Age-related macular degeneration and smoking: the Rotterdam study[J]. Arch Ophthalmol, 1996, 114(10): 1193-1196. DOI: 10.1001/archopht.1996.01100140393005.
9.	Delcourt P, Diaz JL, Ponton-Sanchez A, et al. Smoking and age-related macular degeneration: the POLA study[J]. Arch Ophthalmol, 1998, 116(8): 1031-1035. DOI: 10.1001/archopht.116.8.1031.
10.	Davis SJ, Lyzogubov VV, Tytarenko RG, et al. The effect of nicotine on anti-vascular endothelial growth factor therapy in a mouse model of neovascular age-related macular degeneration[J]. Retina, 2012, 32(6): 1171-1180. DOI: 10.1097/IAE.0b013e31823496b8.
11.	Lee S, Song SJ, Yu HG. Current smoking is associated with a poor visual acuity improvement after intravitreal ranibizumab therapy in patients with exudative age-related macular degeneration[J]. J Korean Med Sci, 2013, 28(5): 769-774. DOI: 10.3346/jkms.2013.28.5.769.
12.	Sharma G, Vijayaraghavan S. Nicotinic receptor signaling in nonexcitable cells[J]. J Neurobiol, 2002, 53(4): 524-534. DOI: 10.1002/neu.10114.
13.	Leonard S, Bertrand D. Neuronal nicotinic receptors: from structure to function[J]. Nicotine Tob Res, 2001, 3(3): 203-223. DOI: 10.1080/14622200110050213.
14.	Lee J, Cooke JP. Nicotine and pathological angiogenes[J]. Life Sci, 2012, 91(21-22): 1058-1064. DOI: 10.1016/j.lfs.2012.06.032.
15.	Karlin A, Akabas MH. Toward astructural basis for the function ofnicotinic acetylcholine receptors and their cousins[J]. Neuron, 1995, 15(6): 1231-1244. DOI: 10.1016/0896-6273(95)90004-7.
16.	Villablanca AC. Nicotine stimulates DNA synthesis and proliferation in vascular endothelial cells in vitro[J]. J Appl Physiol, 1998, 84(6): 2089-2098. DOI: 10.1152/jappl.1998.84.6.2089.
17.	Macklin KD, Maus AD, Pereira EF, et al. Human vascular endothelial cells express functional nicotinic acetylcholine receptors[J]. J Pharmacol Exp Ther, 1998, 287(1): 435-439. DOI: 10.1002/pits.20297.
18.	Grando SA, Horton RM, Pereira EF, et al. A nicotinic acetylcholine receptor regulating cell adhesion and motility is expressed in human keratinocytes[J]. J Invest Dermatol, 1995, 105(6): 774-781. DOI: 10.1111/1523-1747.ep12325606.
19.	Richman DP, Arnason BG. Nicotinic acetylcholine receptor: evidence for a functionally distinct receptor on human lymphocytes[J]. Proc Natl Acad Sci USA, 1979, 76(9): 4632-4635. DOI: 10.1073/pnas.76.9.4632.
20.	Pons M, Marincastano ME. Nicotine increases the VEGF/PEDF ratio in retinal pigment epithelium: a possible mechanism for CNV in passive smokers with AMD[J]. Invest Ophthalmol Vis Sci, 2011, 52(6): 3842-3853. DOI: 10.1167/iovs.10-6254.
21.	Wu JC, Chruscinski A, De Jesus Perez VA, et al. Cholinergic modulation of angiogenesis: role of the 7 nicotinic acetylcholine receptor[J]. J Cell Biochem, 2010, 108(2): 433-446. DOI: 10.1002/jcb.22270.
22.	Shao Z, Yakel JL. Single channel properties of neuronal nicotinic ACh receptors in stratum radiatum interneurons of rat hippocampal slices[J]. J physiol, 2000, 527(3): 507-513. DOI: 10.1111/j.1469-7793.2000.00507.x.
23.	Firth AL, Remillard CV, Yuan JX. TRP channels in hypertension[J]. Biochim Biophys Acta, 2007, 1772(8): 895-906. DOI: 10.1016/j.bbadis.2007.02.009.
24.	Nilius B, Droogmans G, Wondergem R. Transient receptor potential channels in endothelium: solving the calcium entry puzzle?[J]. Endothelium, 2003, 10(1): 5-15. DOI: 10.1080/10623320303356.
25.	Heeschen C, Weis M, Aicher A, et al. A novel angiogenic pathway mediated by non-neuronal nicotinic acetylcholine receptors[J]. J Clin Invest, 2002, 110(4): 527-536. DOI: 10.1172/JCI14676.
26.	Brown KC, Lau JK, Dom AM, et al. MG624, an alpha7-nAChR antagonist, inhibits angiogenesis via the Egr-1/FGF2 pathway[J]. Angiogenesis, 2012, 15(1): 99-114. DOI: 10.1007/s10456-011-9246-9.
27.	Dom AM, Buckley AW, Brown KC, et al. The alpha7-nicotinic acetylcholine receptor and MMP-2/-9 pathway mediate the proangiogenic effect of nicotine in human retinal endothelial cells[J]. Invest Ophthalmol Vis Sci, 2011, 52(7): 4428-4438. DOI: 10.1167/iovs.10-5461.
28.	Kwak N, Okamoto N, Wood JM, et al. VEGF is major stimulator in model of choroidal neovascularization[J]. Invest Ophthalmol Vis Sci, 2000, 41(10): 3158-3164. DOI: 10.1680/nuen.40.4.223.39336.
29.	Ohno-Matsui K, Morita I, Tombran-Tink J, et al. Novel mechanism for age-related macular degeneration: an equilibrium shift between the angiogenesis factors VEGF and PEDF[J]. J Cell Physiol, 2001, 189(3): 323-333. DOI: 10.1002/jcp.10026.
30.	Kurzen H, Wessler I, Kirkpatrick CJ, et al. The non-neuronal cholinergic system of human skin[J]. Horm Metab Res, 2007, 39(2): 125-135. DOI: 10.1055/s-2007-961816.
31.	Ng MK, Wu J, Chang E, et al. A central role for nicotinic cholinergic regulation of growth factor-induced endothelial cell migration[J]. Arterioscler Thromb Vasc Biol, 2007, 27(1): 106-112. DOI: 10.1161/01.ATV.0000251517.98396.4a.
32.	Asahara T, Takahashi T, Masuda H, et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells[J]. EMBO J, 2014, 18(14): 3964-3972. DOI: 10.1093/emboj/18.14.3964.
33.	Crosby JR, Kaminski WE, Schatteman G, et al. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation[J]. Circ Res, 2000, 87(9): 728-730. DOI: 10.1161/01.RES.87.9.728.
34.	Heeschen C, Chang E, Aicher A, et al. Endothelial progenitor cells participate in nicotine-mediated angiogenesis[J]. J Am Coll Cardiol, 2006, 48(12): 2553-2560. DOI: 10.1016/j.jacc.2006.07.066.
35.	Sheridan CM, Rice D, Hiscott PS, et al. The presence of AC133-positive cells suggests a possible role of endothelial progenitor cells in the formation of choroidal neovascularization[J]. Invest Ophthalmol Vis Sci, 2006, 47(4): 1642-1645. DOI: 10.1167/iovs.05-0779.
36.	Hou HY, Wang YS, Xu JF, et al. The dynamic conduct of bone marrow-derived cells in the choroidal neovascularization microenvironment[J]. Curr Eye Res, 2006, 31(12): 1051-1061. DOI: 10.1080/02713680601100459.
37.	Csaky KG, Baffi JZ, Byrnes GA, et al. Recruitment of marrow-derived endothelial cells to experimental choroidal neovascularization by local expression of vascular endothelial growth factor[J]. Exp Eye Res, 2004, 78(6): 1107-1116. DOI: 10.1016/j.exer.2004.01.010.
38.	Caicedo A, Espinosa-Heidmann DG, Pina Y, et al. Blood-derived macrophages infiltrate the retina and activate Muller glial cells under experimental choroidal neovascularization[J]. Exp Eye Res, 2005, 81(1): 38-47. DOI: 10.1016/j.exer.2005.01.013.
39.	Hou YU, Wang YS, Xu JF, et al. Nicotine promotes contribution of bone marrow-derived cells to experimental choroidal neovascularization in mice[J]. Exp Eye Res, 2008, 86(6): 983. DOI: 10.1016/j.exer.2008.03.018.
40.	Johnson LV, Leitner WP, Staples MK, et al. Complement activation and inflammatory process in dursen formation and age-related macular degeneration[J]. Exp Eye Res, 2001, 73(6): 887-896. DOI: 10.1006/exer.2001.1094.
41.	Bora PS, Sohn JH, Cruz JM, et al. Role of complement and complement membrane attack complex in laser-induced choroidal neovascularization[J]. J Immunol, 2005, 174(1): 491-497. DOI: 10.1016/j.ajo.2005.03.011.
42.	Bora NS, Kaliappan S, Jha P, et al. Complement activation via alternative pathway is critical in the development of laser-induced choroidal neovascularization: role of factor B and factor H[J]. J Immunol, 2006, 177(3): 1872-1878. DOI: 10.4049/jimmunol.177.3.1872.
43.	Bora NS, Kaliappan S, Jha P, et al. CD59, a complement regulatory protein, controls choroidal neovascularization in a mouse model of wet-type age-related macular degeneration[J]. J Immunol, 2007, 178(3): 1783-1790. DOI: 10.4049/jimmunol.178.3.1783.
44.	Woodell A, Rohrer B. A mechanistic review of cigarette smoke and age-related macular degeneration[J]. Adv Exp Med Biol, 2014, 801: 301-307. DOI: 10.1007/978-1-4614-3209-8_38.
45.	Yu AL, Birke K, Burger J, et al. Biological effects of cigarette smoke in cultured human retinal pigment epithelial cells[J/OL]. PLoS One, 2012, 7(11): 48501[2012-11-14]. https://doi.org/10.1371/journal.pone.0048501. DOI: 10.1371/journal.pone.0048501.
46.	Li H, Yang T, Ning Q, et al. Cigarette smoke extract-treated mast cells promote alveolar macrophage infiltration and polarization in experimental chronic obstructive pulmonary disease[J]. Inhal Toxicol, 2015, 27(14): 822-831. DOI: 10.3109/08958378.2015.1116644.
47.	Krause TA, Alex AF, Engel DR, et al. VEGF-production by CCR2-dependent macrophages contributes to laser-induced choroidal neovascularization[J/OL]. PLoS One 2014, 9(4): 94313[2014-4-8]. https://doi.org/10.1371/journal.pone.0094313. DOI: 10.1371/journal.pone.0094313.
48.	Liu J, Copland DA, Theodoropoulou S, et al. Impairing autophagy in retinal pigment epithelium leads to inflammasome activation and enhanced macrophage-mediated angiogenesis[J]. Sci Rep, 2016, 6: 20639[2016-02-05]. http://dx.doi.org/10.1038/srep20639. DOI: 10.1038/srep20639.
49.	Sastry BV, Hemontolor ME. Influence of nicotine and cotinine on retinal phospholipase A2 and its significance to macular function[J]. J Ocul Pharmacol Ther, 1998, 14(5): 447-458. DOI: 10.1089/jop.1998.14.447.
50.	Brogan AP, Dickerson TJ, Boldt GE, et al. Altered retinoid homeostasis catalyzed by a nicotine metabolite: implications in macular degeneration and normal development[J]. Proc Natl Acad Sci USA, 2005, 102(30): 10433-10438. DOI: 10.1073/pnas.0504721102.
51.	Maugeri G, D'Amico AG, Rasà DM, et al. Nicotine promotes blood retinal barrier damage in a model of human diabetic macular edema[J]. Toxicol In Vitro, 2017, 44(3): 182-189. DOI: 10.1016/j.tiv.2017.07.003.

1. Lim LS, Mitch P, Seddon JM, et al. Age-related macular degeneration[J]. Lancet, 2012, 379(9827): 1728-1738. DOI: 10.1016/S0140-6736(12)60282-7.
2. Shao J, Choudhary MM, Schachat AP, et al. Neovascular age-related macular degeneration[J]. Dev Ophthalmol, 2016, 55: 125-136. DOI: 10.1159/000438969.
3. Velilla S, Garcia-Medina JJ, Garcia-Layana A, et al. Smoking and age-related macular degeneration: review and update[J/OL]. J Ophthalmol, 2013, 2013: 895147[2013-12-04]. https://dx.doi.org/10.1155/2013/895147. DOI: 10.1155/2013/895147.
4. Moracco KE, Morgan JC, Mendel J, et al. "My first thought was croutons": perceptions of cigarettes and cigarette smoke constituents among adult smokers and nonsmokers[J]. Nicotine Tob Res, 2015, 18(7): 1566-1574. DOI: 10.1093/ntr/ntv281.
5. Willeford KT, Rapp J. Smoking and age-related macular degeneration: biochemical mechanisms and patient support[J]. Optom Vis Sci, 2012, 89(11): 1662-1666. DOI: 10.1097/OPX.0b013e31826c5df2.
6. Suner IJ, Hernandez EP, Espinosaheidmann DG, et al. Nicotine increases size and severity of experimental choroidal neovascularization[J]. Invest Ophthalmol Vis Sci, 2004, 45(1): 311-317. DOI: 10.1167/iovs.03-0733.
7. Lechanteur YT, VandeCamp PL, Smailhodzic D, et al. Association of smoking and CFH and ARMS2 risk variants with younger age at onset of neovascular age-related macular degeneration[J]. JAMA Ophthalmol, 2015, 133(5): 533-541. DOI: 10.1001/jamaophthalmol.2015.18.
8. Vingerling JR, Hofman A, Grobbee DE, et al. Age-related macular degeneration and smoking: the Rotterdam study[J]. Arch Ophthalmol, 1996, 114(10): 1193-1196. DOI: 10.1001/archopht.1996.01100140393005.
9. Delcourt P, Diaz JL, Ponton-Sanchez A, et al. Smoking and age-related macular degeneration: the POLA study[J]. Arch Ophthalmol, 1998, 116(8): 1031-1035. DOI: 10.1001/archopht.116.8.1031.
10. Davis SJ, Lyzogubov VV, Tytarenko RG, et al. The effect of nicotine on anti-vascular endothelial growth factor therapy in a mouse model of neovascular age-related macular degeneration[J]. Retina, 2012, 32(6): 1171-1180. DOI: 10.1097/IAE.0b013e31823496b8.
11. Lee S, Song SJ, Yu HG. Current smoking is associated with a poor visual acuity improvement after intravitreal ranibizumab therapy in patients with exudative age-related macular degeneration[J]. J Korean Med Sci, 2013, 28(5): 769-774. DOI: 10.3346/jkms.2013.28.5.769.
12. Sharma G, Vijayaraghavan S. Nicotinic receptor signaling in nonexcitable cells[J]. J Neurobiol, 2002, 53(4): 524-534. DOI: 10.1002/neu.10114.
13. Leonard S, Bertrand D. Neuronal nicotinic receptors: from structure to function[J]. Nicotine Tob Res, 2001, 3(3): 203-223. DOI: 10.1080/14622200110050213.
14. Lee J, Cooke JP. Nicotine and pathological angiogenes[J]. Life Sci, 2012, 91(21-22): 1058-1064. DOI: 10.1016/j.lfs.2012.06.032.
15. Karlin A, Akabas MH. Toward astructural basis for the function ofnicotinic acetylcholine receptors and their cousins[J]. Neuron, 1995, 15(6): 1231-1244. DOI: 10.1016/0896-6273(95)90004-7.
16. Villablanca AC. Nicotine stimulates DNA synthesis and proliferation in vascular endothelial cells in vitro[J]. J Appl Physiol, 1998, 84(6): 2089-2098. DOI: 10.1152/jappl.1998.84.6.2089.
17. Macklin KD, Maus AD, Pereira EF, et al. Human vascular endothelial cells express functional nicotinic acetylcholine receptors[J]. J Pharmacol Exp Ther, 1998, 287(1): 435-439. DOI: 10.1002/pits.20297.
18. Grando SA, Horton RM, Pereira EF, et al. A nicotinic acetylcholine receptor regulating cell adhesion and motility is expressed in human keratinocytes[J]. J Invest Dermatol, 1995, 105(6): 774-781. DOI: 10.1111/1523-1747.ep12325606.
19. Richman DP, Arnason BG. Nicotinic acetylcholine receptor: evidence for a functionally distinct receptor on human lymphocytes[J]. Proc Natl Acad Sci USA, 1979, 76(9): 4632-4635. DOI: 10.1073/pnas.76.9.4632.
20. Pons M, Marincastano ME. Nicotine increases the VEGF/PEDF ratio in retinal pigment epithelium: a possible mechanism for CNV in passive smokers with AMD[J]. Invest Ophthalmol Vis Sci, 2011, 52(6): 3842-3853. DOI: 10.1167/iovs.10-6254.
21. Wu JC, Chruscinski A, De Jesus Perez VA, et al. Cholinergic modulation of angiogenesis: role of the 7 nicotinic acetylcholine receptor[J]. J Cell Biochem, 2010, 108(2): 433-446. DOI: 10.1002/jcb.22270.
22. Shao Z, Yakel JL. Single channel properties of neuronal nicotinic ACh receptors in stratum radiatum interneurons of rat hippocampal slices[J]. J physiol, 2000, 527(3): 507-513. DOI: 10.1111/j.1469-7793.2000.00507.x.
23. Firth AL, Remillard CV, Yuan JX. TRP channels in hypertension[J]. Biochim Biophys Acta, 2007, 1772(8): 895-906. DOI: 10.1016/j.bbadis.2007.02.009.
24. Nilius B, Droogmans G, Wondergem R. Transient receptor potential channels in endothelium: solving the calcium entry puzzle?[J]. Endothelium, 2003, 10(1): 5-15. DOI: 10.1080/10623320303356.
25. Heeschen C, Weis M, Aicher A, et al. A novel angiogenic pathway mediated by non-neuronal nicotinic acetylcholine receptors[J]. J Clin Invest, 2002, 110(4): 527-536. DOI: 10.1172/JCI14676.
26. Brown KC, Lau JK, Dom AM, et al. MG624, an alpha7-nAChR antagonist, inhibits angiogenesis via the Egr-1/FGF2 pathway[J]. Angiogenesis, 2012, 15(1): 99-114. DOI: 10.1007/s10456-011-9246-9.
27. Dom AM, Buckley AW, Brown KC, et al. The alpha7-nicotinic acetylcholine receptor and MMP-2/-9 pathway mediate the proangiogenic effect of nicotine in human retinal endothelial cells[J]. Invest Ophthalmol Vis Sci, 2011, 52(7): 4428-4438. DOI: 10.1167/iovs.10-5461.
28. Kwak N, Okamoto N, Wood JM, et al. VEGF is major stimulator in model of choroidal neovascularization[J]. Invest Ophthalmol Vis Sci, 2000, 41(10): 3158-3164. DOI: 10.1680/nuen.40.4.223.39336.
29. Ohno-Matsui K, Morita I, Tombran-Tink J, et al. Novel mechanism for age-related macular degeneration: an equilibrium shift between the angiogenesis factors VEGF and PEDF[J]. J Cell Physiol, 2001, 189(3): 323-333. DOI: 10.1002/jcp.10026.
30. Kurzen H, Wessler I, Kirkpatrick CJ, et al. The non-neuronal cholinergic system of human skin[J]. Horm Metab Res, 2007, 39(2): 125-135. DOI: 10.1055/s-2007-961816.
31. Ng MK, Wu J, Chang E, et al. A central role for nicotinic cholinergic regulation of growth factor-induced endothelial cell migration[J]. Arterioscler Thromb Vasc Biol, 2007, 27(1): 106-112. DOI: 10.1161/01.ATV.0000251517.98396.4a.
32. Asahara T, Takahashi T, Masuda H, et al. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells[J]. EMBO J, 2014, 18(14): 3964-3972. DOI: 10.1093/emboj/18.14.3964.
33. Crosby JR, Kaminski WE, Schatteman G, et al. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation[J]. Circ Res, 2000, 87(9): 728-730. DOI: 10.1161/01.RES.87.9.728.
34. Heeschen C, Chang E, Aicher A, et al. Endothelial progenitor cells participate in nicotine-mediated angiogenesis[J]. J Am Coll Cardiol, 2006, 48(12): 2553-2560. DOI: 10.1016/j.jacc.2006.07.066.
35. Sheridan CM, Rice D, Hiscott PS, et al. The presence of AC133-positive cells suggests a possible role of endothelial progenitor cells in the formation of choroidal neovascularization[J]. Invest Ophthalmol Vis Sci, 2006, 47(4): 1642-1645. DOI: 10.1167/iovs.05-0779.
36. Hou HY, Wang YS, Xu JF, et al. The dynamic conduct of bone marrow-derived cells in the choroidal neovascularization microenvironment[J]. Curr Eye Res, 2006, 31(12): 1051-1061. DOI: 10.1080/02713680601100459.
37. Csaky KG, Baffi JZ, Byrnes GA, et al. Recruitment of marrow-derived endothelial cells to experimental choroidal neovascularization by local expression of vascular endothelial growth factor[J]. Exp Eye Res, 2004, 78(6): 1107-1116. DOI: 10.1016/j.exer.2004.01.010.
38. Caicedo A, Espinosa-Heidmann DG, Pina Y, et al. Blood-derived macrophages infiltrate the retina and activate Muller glial cells under experimental choroidal neovascularization[J]. Exp Eye Res, 2005, 81(1): 38-47. DOI: 10.1016/j.exer.2005.01.013.
39. Hou YU, Wang YS, Xu JF, et al. Nicotine promotes contribution of bone marrow-derived cells to experimental choroidal neovascularization in mice[J]. Exp Eye Res, 2008, 86(6): 983. DOI: 10.1016/j.exer.2008.03.018.
40. Johnson LV, Leitner WP, Staples MK, et al. Complement activation and inflammatory process in dursen formation and age-related macular degeneration[J]. Exp Eye Res, 2001, 73(6): 887-896. DOI: 10.1006/exer.2001.1094.
41. Bora PS, Sohn JH, Cruz JM, et al. Role of complement and complement membrane attack complex in laser-induced choroidal neovascularization[J]. J Immunol, 2005, 174(1): 491-497. DOI: 10.1016/j.ajo.2005.03.011.
42. Bora NS, Kaliappan S, Jha P, et al. Complement activation via alternative pathway is critical in the development of laser-induced choroidal neovascularization: role of factor B and factor H[J]. J Immunol, 2006, 177(3): 1872-1878. DOI: 10.4049/jimmunol.177.3.1872.
43. Bora NS, Kaliappan S, Jha P, et al. CD59, a complement regulatory protein, controls choroidal neovascularization in a mouse model of wet-type age-related macular degeneration[J]. J Immunol, 2007, 178(3): 1783-1790. DOI: 10.4049/jimmunol.178.3.1783.
44. Woodell A, Rohrer B. A mechanistic review of cigarette smoke and age-related macular degeneration[J]. Adv Exp Med Biol, 2014, 801: 301-307. DOI: 10.1007/978-1-4614-3209-8_38.
45. Yu AL, Birke K, Burger J, et al. Biological effects of cigarette smoke in cultured human retinal pigment epithelial cells[J/OL]. PLoS One, 2012, 7(11): 48501[2012-11-14]. https://doi.org/10.1371/journal.pone.0048501. DOI: 10.1371/journal.pone.0048501.
46. Li H, Yang T, Ning Q, et al. Cigarette smoke extract-treated mast cells promote alveolar macrophage infiltration and polarization in experimental chronic obstructive pulmonary disease[J]. Inhal Toxicol, 2015, 27(14): 822-831. DOI: 10.3109/08958378.2015.1116644.
47. Krause TA, Alex AF, Engel DR, et al. VEGF-production by CCR2-dependent macrophages contributes to laser-induced choroidal neovascularization[J/OL]. PLoS One 2014, 9(4): 94313[2014-4-8]. https://doi.org/10.1371/journal.pone.0094313. DOI: 10.1371/journal.pone.0094313.
48. Liu J, Copland DA, Theodoropoulou S, et al. Impairing autophagy in retinal pigment epithelium leads to inflammasome activation and enhanced macrophage-mediated angiogenesis[J]. Sci Rep, 2016, 6: 20639[2016-02-05]. http://dx.doi.org/10.1038/srep20639. DOI: 10.1038/srep20639.
49. Sastry BV, Hemontolor ME. Influence of nicotine and cotinine on retinal phospholipase A2 and its significance to macular function[J]. J Ocul Pharmacol Ther, 1998, 14(5): 447-458. DOI: 10.1089/jop.1998.14.447.
50. Brogan AP, Dickerson TJ, Boldt GE, et al. Altered retinoid homeostasis catalyzed by a nicotine metabolite: implications in macular degeneration and normal development[J]. Proc Natl Acad Sci USA, 2005, 102(30): 10433-10438. DOI: 10.1073/pnas.0504721102.
51. Maugeri G, D'Amico AG, Rasà DM, et al. Nicotine promotes blood retinal barrier damage in a model of human diabetic macular edema[J]. Toxicol In Vitro, 2017, 44(3): 182-189. DOI: 10.1016/j.tiv.2017.07.003.

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