Review Article

Growth Factors as Tools in Photoreceptor Cell Regeneration and Vision Recovery

Author(s): Fatemeh Forouzanfar, Mana Shojapour, Zahra Sadat Aghili and Samira Asgharzade*

Volume 21, Issue 6, 2020

Page: [573 - 581] Pages: 9

DOI: 10.2174/1389450120666191121103831

Price: $65

Abstract

Photoreceptor loss is a major cause of blindness around the world. Stem cell therapy offers a new strategy in retina degenerative disease. Retinal progenitors can be derived from embryonic stem cells (ESC) in vitro, but cannot be processed to a mature state. In addition, the adult recipient retina presents a very different environment than the photoreceptor precursor donor.

It seems that modulation of the recipient environment by ectopic development regulated growth factors for transplanted cells could generate efficient putative photoreceptors. The purpose of this review article was to investigate the signaling pathway of growth factors including: insulin-like growth factors (IGFs), fibroblast growth factors (FGF), Nerve growth factor (NGF), Brain-derived neurotrophic factor (BDNF), Taurin and Retinoic acid (RA) involved in the differentiation of neuroretina cell, like; photoreceptor and retinal progenitor cells. Given the results available in the related literature, the differentiation efficacy of ESCs toward the photoreceptor and retinal neurons and the important role of growth factors in activating signaling pathways such as Akt, Ras/Raf1/ and ERKs also inhibit the ASK1/JNK apoptosis pathway. Manipulating differentiated culture, growth factors can influence photoreceptor transplantation efficiency in retinal degenerative disease.

Keywords: Differentiation, embryonic stem cells, growth factor, photoreceptor, fibroblast, taurin and Retinoic Acid (RA).

Graphical Abstract

[1]
West, E.L.; Pearson, R.A.; Duran, Y. Manipulation of the recipient retinal environment by ectopic expression of neurotrophic growth factors can improve transplanted photoreceptor integration and survival. Cell Transplant., 2012, 21(5), 871-887.
[http://dx.doi.org/10.3727/096368911X623871] [PMID: 22325046]
[2]
Chaum, E. Retinal neuroprotection by growth factors: a mechanistic perspective. J. Cell. Biochem., 2003, 88(1), 57-75.
[http://dx.doi.org/10.1002/jcb.10354] [PMID: 12461775]
[3]
Arroba, A.I.; Alvarez-Lindo, N.; van Rooijen, N.; de la Rosa, E.J. Microglia-mediated IGF-I neuroprotection in the rd10 mouse model of retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci., 2011, 52(12), 9124-9130.
[http://dx.doi.org/10.1167/iovs.11-7736] [PMID: 22039242]
[4]
Daly, C.; Ward, R.; Reynolds, A.L.; Galvin, O.; Collery, R.F.; Kennedy, B.N. Brain-derived neurotrophic factor as a treatment option for retinal degeneration. Adv. Exp. Med. Biol., 2018, 1074, 465-471.
[http://dx.doi.org/10.1007/978-3-319-75402-4_57] [PMID: 29721977]
[5]
De Genaro, P.; Simón, M.V.; Rotstein, N.P.; Politi, L.E. Retinoic acid promotes apoptosis and differentiation in photoreceptors by activating the P38 MAP kinase pathway. Invest. Ophthalmol. Vis. Sci., 2013, 54(5), 3143-3156.
[http://dx.doi.org/10.1167/iovs.12-11049] [PMID: 23580485]
[6]
Gaucher, D; Arnault, E; Husson, Z; Froger, N; Dubus, E; Gondouin, P et al. Taurine deficiency damages retinal neurones: cone photoreceptors and retinal ganglion cells 2012; 43(5)1979
[http://dx.doi.org/10.1007/s00726-012-1273-3]
[7]
Hirami, Y.; Osakada, F.; Takahashi, K. Generation of retinal cells from mouse and human induced pluripotent stem cells. Neurosci. Lett., 2009, 458(3), 126-131.
[http://dx.doi.org/10.1016/j.neulet.2009.04.035] [PMID: 19379795]
[8]
Adão-Novaes, J.; de Cássia Belem Guterrres, C.; Linden, R.; Sholl-Franco, A. Rod photoreceptor cell death is induced by okadaic acid through activation of PKC and L-type voltage-dependent Ca2+ channels and prevented by IGF-1. Neurochem. Int., 2010, 57(2), 128-135.
[http://dx.doi.org/10.1016/j.neuint.2010.04.021] [PMID: 20466029]
[9]
Mellough, C.B.; Collin, J.; Khazim, M. IGF-1 Signaling plays an important role in the formation of three-dimensional laminated neural retina and other ocular structures from human embryonic stem cells. Stem Cells, 2015, 33(8), 2416-2430.
[http://dx.doi.org/10.1002/stem.2023] [PMID: 25827910]
[10]
Narayan, D.S.; Wood, J.P.; Chidlow, G.; Casson, R.J. A review of the mechanisms of cone degeneration in retinitis pigmentosa. Acta Ophthalmol., 2016, 94(8), 748-754.
[http://dx.doi.org/10.1111/aos.13141] [PMID: 27350263]
[11]
Okunuki, Y; Mukai, R; Pearsall, EA; Klokman, G; Husain, D; Park, D-H Microglia inhibit photoreceptor cell death and regulate immune cell infiltration in response to retinal detachment, 2018. 115(27): E6264-73.
[http://dx.doi.org/10.1073/pnas.1719601115]
[12]
Cameron, DA Easter SJJoN., Cone photoreceptor regeneration in adult fish retina: phenotypic determination and mosaic pattern formation 1995; 15(3): 2255-71.
[13]
Kruczek, K.; Gonzalez-Cordero, A.; Goh, D. Differentiation and transplantation of embryonic stem cell-derived cone photoreceptors into a mouse model of end-stage retinal degeneration. Stem Cell Reports, 2017, 8(6), 1659-1674.
[http://dx.doi.org/10.1016/j.stemcr.2017.04.030] [PMID: 28552606]
[14]
Azadi, S.; Johnson, L.E.; Paquet-Durand, F. CNTF+BDNF treatment and neuroprotective pathways in the rd1 mouse retina. Brain Res., 2007, 1129(1), 116-129.
[http://dx.doi.org/10.1016/j.brainres.2006.10.031] [PMID: 17156753]
[15]
Jin, W; Xing, Y-q Epidermal growth factor promotes the differentiation of stem cells derived from human umbilical cord blood into neuron-like cells via taurine induction in vitro.2009; 45(7)321
[16]
Tomi, M; Terayama, T; Isobe, T; Egami, F; Morito, A; Kurachi, M Function and regulation of taurine transport at the inner blood–retinal barrier, 2007. 73(2): 100-6.
[http://dx.doi.org/10.1016/j.mvr.2006.10.003]
[17]
Li, X-W; Gao, H-Y Liu JJNn., The role of taurine in improving neural stem cells proliferation and differentiation 2017; 20(7): 409- 15.
[18]
Hayes, K.C.; Trautwein, E.A. Taurine deficiency syndrome in cats. Vet. Clin. North Am. Small Anim. Pract., 1989, 19(3), 403-413.
[http://dx.doi.org/10.1016/S0195-5616(89)50052-4] [PMID: 2658282]
[19]
Hernández-Benítez, R; Ramos-Mandujano, G Pasantes-Morales HJScr., Taurine stimulates proliferation and promotes neurogenesis of mouse adult cultured neural stem/progenitor cells 2012; 9(1): 24-34.
[20]
Froger, N.; Cadetti, L.; Lorach, H. Taurine provides neuroprotection against retinal ganglion cell degeneration. PLoS One, 2012, 7(10)e42017
[http://dx.doi.org/10.1371/journal.pone.0042017] [PMID: 23115615]
[21]
Hadj-Saïd, W.; Fradot, V.; Ivkovic, I.; Sahel, J.A.; Picaud, S.; Froger, N. Taurine Promotes Retinal Ganglion Cell Survival Through GABAB Receptor Activation. Adv. Exp. Med. Biol., 2017, 975(Pt 2), 687-701.
[http://dx.doi.org/10.1007/978-94-024-1079-2_54] [PMID: 28849492]
[22]
Militante, J.D.; Lombardini, J.B. Pharmacological characterization of the effects of taurine on calcium uptake in the rat retina. Amino Acids, 1998, 15(1-2), 99-108.
[http://dx.doi.org/10.1007/BF01345283] [PMID: 9871490]
[23]
Lambuk, L.; Iezhitsa, I.; Agarwal, R.; Bakar, N.S.; Agarwal, P.; Ismail, N.M. Antiapoptotic effect of taurine against NMDA-induced retinal excitotoxicity in rats. Neurotoxicology, 2019, 70, 62-71.
[http://dx.doi.org/10.1016/j.neuro.2018.10.009] [PMID: 30385388]
[24]
Sun, M.; Xu, C. Neuroprotective mechanism of taurine due to up-regulating calpastatin and down-regulating calpain and caspase-3 during focal cerebral ischemia. Cell. Mol. Neurobiol., 2008, 28(4), 593-611.
[http://dx.doi.org/10.1007/s10571-007-9183-8] [PMID: 17712625]
[25]
Das, B.C.; Thapa, P.; Karki, R. Retinoic acid signaling pathways in development and diseases. Bioorg. Med. Chem., 2014, 22(2), 673-683.
[http://dx.doi.org/10.1016/j.bmc.2013.11.025] [PMID: 24393720]
[26]
di Masi, A.; Leboffe, L.; De Marinis, E. Retinoic acid receptors: from molecular mechanisms to cancer therapy. Mol. Aspects Med., 2015, 41, 1-115.
[http://dx.doi.org/10.1016/j.mam.2014.12.003] [PMID: 25543955]
[27]
Larange, A.; Cheroutre, H. Retinoic acid and retinoic acid receptors as pleiotropic modulators of the immune system. Annu. Rev. Immunol., 2016, 34, 369-394.
[http://dx.doi.org/10.1146/annurev-immunol-041015-055427] [PMID: 27168242]
[28]
Janssen, J.J.; Kuhlmann, E.D.; van Vugt, A.H. Retinoic acid receptors and retinoid X receptors in the mature retina: subtype determination and cellular distribution. Curr. Eye Res., 1999, 19(4), 338-347.
[http://dx.doi.org/10.1076/ceyr.19.4.338.5307] [PMID: 10520230]
[29]
Rowe, A.; Brickell, P.M. The nuclear retinoid receptors. Int. J. Exp. Pathol., 1993, 74(2), 117-126.
[PMID: 8388706]
[30]
Khanna, H.; Akimoto, M.; Siffroi-Fernandez, S.; Friedman, J.S.; Hicks, D.; Swaroop, A. Retinoic acid regulates the expression of photoreceptor transcription factor NRL. J. Biol. Chem., 2006, 281(37), 27327-27334.
[http://dx.doi.org/10.1074/jbc.M605500200] [PMID: 16854989]
[31]
Hale, F. PIGS BORN WITHOUT EYE BALLS. J. Hered., 1933, 24(3), 105-106.
[http://dx.doi.org/10.1093/oxfordjournals.jhered.a103720]
[32]
Hale, F. The Relation of Vitamin a to Anophthalmos in Pigs. Am. J. Ophthalmol., 1935, 18(12), 1087-1093.
[http://dx.doi.org/10.1016/S0002-9394(35)90563-3]
[33]
Wang, W-D.; Hsu, H-J.; Li, Y-F.; Wu, C-Y. Retinoic acid protects and rescues the development of zebrafish embryonic retinal photoreceptor cells from exposure to paclobutrazol. Int. J. Mol. Sci., 2017, 18(1), 130.
[http://dx.doi.org/10.3390/ijms18010130] [PMID: 28085063]
[34]
Duester, G. Keeping an eye on retinoic acid signaling during eye development. Chem. Biol. Interact., 2009, 178(1-3), 178-181.
[http://dx.doi.org/10.1016/j.cbi.2008.09.004] [PMID: 18831967]
[35]
Cvekl, A.; Wang, W.L. Retinoic acid signaling in mammalian eye development. Exp. Eye Res., 2009, 89(3), 280-291.
[http://dx.doi.org/10.1016/j.exer.2009.04.012] [PMID: 19427305]
[36]
Kelley, M.W.; Turner, J.K.; Reh, T.A. Retinoic acid promotes differentiation of photoreceptors in vitro. Development, 1994, 120(8), 2091-2102.
[PMID: 7925013]
[37]
Hyatt, G.A.; Schmitt, E.A.; Fadool, J.M.; Dowling, J.E. Retinoic acid alters photoreceptor development in vivo. Proc. Natl. Acad. Sci. USA, 1996, 93(23), 13298-13303.
[http://dx.doi.org/10.1073/pnas.93.23.13298] [PMID: 8917585]
[38]
Stull, D.L.; Wikler, K.C. Retinoid-dependent gene expression regulates early morphological events in the development of the murine retina. J. Comp. Neurol., 2000, 417(3), 289-298.
[http://dx.doi.org/10.1002/(SICI)1096-9861(20000214)417:3<289:AID-CNE3>3.0.CO;2-S] [PMID: 10683604]
[39]
Hyatt, G.A.; Schmitt, E.A.; Marsh-Armstrong, N.R.; Dowling, J.E. Retinoic acid-induced duplication of the zebrafish retina. Proc. Natl. Acad. Sci. USA, 1992, 89(17), 8293-8297.
[http://dx.doi.org/10.1073/pnas.89.17.8293] [PMID: 1518861]
[40]
Biehlmaier, O.; Lampert, J.M.; von Lintig, J.; Kohler, K. Photoreceptor morphology is severely affected in the beta,beta-carotene-15,15′-oxygenase (bcox) zebrafish morphant. Eur. J. Neurosci., 2005, 21(1), 59-68.
[http://dx.doi.org/10.1111/j.1460-9568.2004.03830.x] [PMID: 15654843]
[41]
Ji, H.P.; Xiong, Y.; Zhang, E.D. Which has more stem-cell characteristics: Müller cells or Müller cells derived from in vivo culture in neurospheres? Am. J. Transl. Res., 2017, 9(2), 611-619.
[PMID: 28337288]
[42]
Okazawa, H.; Shimizu, J.; Kamei, M.; Imafuku, I.; Hamada, H.; Kanazawa, I. Bcl-2 inhibits retinoic acid-induced apoptosis during the neural differentiation of embryonal stem cells. J. Cell Biol., 1996, 132(5), 955-968.
[http://dx.doi.org/10.1083/jcb.132.5.955] [PMID: 8603926]
[43]
Falasca, L.; Favale, A.; Gualandi, G.; Maietta, G.; Conti Devirgiliis, L. Retinoic acid treatment induces apoptosis or expression of a more differentiated phenotype on different fractions of cultured fetal rat hepatocytes. Hepatology, 1998, 28(3), 727-737.
[http://dx.doi.org/10.1002/hep.510280319] [PMID: 9731565]
[44]
Szondy, Z.; Reichert, U.; Bernardon, J.M. Inhibition of activation-induced apoptosis of thymocytes by all-trans- and 9-cis-retinoic acid is mediated via retinoic acid receptor alpha. Biochem. J., 1998, 331(Pt 3), 767-774.
[http://dx.doi.org/10.1042/bj3310767] [PMID: 9560303]
[45]
Stenkamp, D.L.; Gregory, J.K.; Adler, R. Retinoid effects in purified cultures of chick embryo retina neurons and photoreceptors. Invest. Ophthalmol. Vis. Sci., 1993, 34(8), 2425-2436.
[PMID: 8325750]
[46]
Söderpalm, A.K.; Fox, D.A.; Karlsson, J.O.; van Veen, T. Retinoic acid produces rod photoreceptor selective apoptosis in developing mammalian retina. Invest. Ophthalmol. Vis. Sci., 2000, 41(3), 937-947.
[PMID: 10711716]
[47]
Golzio, C.; Martinovic-Bouriel, J.; Thomas, S. Matthew-Wood syndrome is caused by truncating mutations in the retinol-binding protein receptor gene STRA6. Am. J. Hum. Genet., 2007, 80(6), 1179-1187.
[http://dx.doi.org/10.1086/518177] [PMID: 17503335]
[48]
Yamamoto, H.; Simon, A.; Eriksson, U.; Harris, E.; Berson, E.L.; Dryja, T.P. Mutations in the gene encoding 11-cis retinol dehydrogenase cause delayed dark adaptation and fundus albipunctatus. Nat. Genet., 1999, 22(2), 188-191.
[http://dx.doi.org/10.1038/9707] [PMID: 10369264]
[49]
Nakamura, M.; Hotta, Y.; Tanikawa, A.; Terasaki, H.; Miyake, Y. A high association with cone dystrophy in Fundus albipunctatus caused by mutations of the RDH5 gene. Invest. Ophthalmol. Vis. Sci., 2000, 41(12), 3925-3932.
[PMID: 11053295]
[50]
Hui, Q.; Jin, Z.; Li, X.; Liu, C.; Wang, X. FGF family: from drug development to clinical application. Int. J. Mol. Sci., 2018, 19(7), 1875.
[http://dx.doi.org/10.3390/ijms19071875] [PMID: 29949887]
[51]
Forouzanfar, F.; Amin, B.; Ghorbani, A. New approach for the treatment of neuropathic pain: Fibroblast growth factor 1 gene-transfected adipose-derived mesenchymal stem cells. Eur. J. Pain, 2018, 22(2), 295-310.
[http://dx.doi.org/10.1002/ejp.1119] [PMID: 28949091]
[52]
Ghazavi, H.; Hoseini, S.J.; Ebrahimzadeh-Bideskan, A. Fibroblast growth factor type 1 (FGF1)-overexpressed adipose-derived mesenchaymal stem cells (AD-MSCFGF1) induce neuroprotection and functional recovery in a rat stroke model. Stem Cell Rev Rep, 2017, 13(5), 670-685.
[http://dx.doi.org/10.1007/s12015-017-9755-z] [PMID: 28795363]
[53]
Hoseini, S.J.; Ghazavi, H.; Forouzanfar, F. Fibroblast growth factor 1-transfected adipose-derived mesenchymal stem cells promote angiogenic proliferation. DNA Cell Biol., 2017, 36(5), 401-412.
[http://dx.doi.org/10.1089/dna.2016.3546] [PMID: 28281780]
[54]
Ornitz, D.M.; Itoh, N. The fibroblast growth factor signaling pathway. Wiley Interdiscip. Rev. Dev. Biol., 2015, 4(3), 215-266.
[http://dx.doi.org/10.1002/wdev.176] [PMID: 25772309]
[55]
Désiré, L.; Head, M.W.; Fayein, N.A.; Courtois, Y.; Jeanny, J.C. Suppression of fibroblast growth factor 2 expression by antisense oligonucleotides inhibits embryonic chick neural retina cell differentiation and survival in vivo. Dev. Dyn., 1998, 212(1), 63-74.
[http://dx.doi.org/10.1002/(SICI)1097-0177(199805)212:1<63:AID-AJA6>3.0.CO;2-0] [PMID: 9603424]
[56]
Fischer, A.J.; Reh, T.A. Growth factors induce neurogenesis in the ciliary body. Dev. Biol., 2003, 259(2), 225-240.
[http://dx.doi.org/10.1016/S0012-1606(03)00178-7] [PMID: 12871698]
[57]
Fontaine, V.; Kinkl, N.; Sahel, J.; Dreyfus, H.; Hicks, D. Survival of purified rat photoreceptors in vitro is stimulated directly by fibroblast growth factor-2. J. Neurosci., 1998, 18(23), 9662-9672.
[http://dx.doi.org/10.1523/JNEUROSCI.18-23-09662.1998] [PMID: 9822727]
[58]
Christopoulos, P.F.; Msaouel, P.; Koutsilieris, M. The role of the insulin-like growth factor-1 system in breast cancer. Mol. Cancer, 2015, 14(1), 43.
[http://dx.doi.org/10.1186/s12943-015-0291-7] [PMID: 25743390]
[59]
Pollak, M. Insulin and insulin-like growth factor signalling in neoplasia. Nat. Rev. Cancer, 2008, 8(12), 915-928.
[http://dx.doi.org/10.1038/nrc2536] [PMID: 19029956]
[60]
LeRoith, D.; Roberts, C.T., Jr The insulin-like growth factor system and cancer. Cancer Lett., 2003, 195(2), 127-137.
[http://dx.doi.org/10.1016/S0304-3835(03)00159-9] [PMID: 12767520]
[61]
Firth, S.M.; Baxter, R.C. Cellular actions of the insulin-like growth factor binding proteins. Endocr. Rev., 2002, 23(6), 824-854.
[http://dx.doi.org/10.1210/er.2001-0033] [PMID: 12466191]
[62]
Hwa, V.; Oh, Y.; Rosenfeld, R.G. The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr. Rev., 1999, 20(6), 761-787.
[http://dx.doi.org/10.1210/er.20.6.761] [PMID: 10605625]
[63]
King, M.; Kelly, L.P.; Wallack, E.M. Serum levels of insulin-like growth factor-1 and brain-derived neurotrophic factor as potential recovery biomarkers in stroke. Neurol. Res., 2019, 41(4), 354-363.
[http://dx.doi.org/10.1080/01616412.2018.1564451] [PMID: 30620251]
[64]
Otteson, D.C.; Cirenza, P.F.; Hitchcock, P.F. Persistent neurogenesis in the teleost retina: evidence for regulation by the growth-hormone/insulin-like growth factor-I axis. Mech. Dev., 2002, 117(1-2), 137-149.
[http://dx.doi.org/10.1016/S0925-4773(02)00188-0] [PMID: 12204254]
[65]
Adão-Novaes, J J, Guterrres CdCB, Linden R, Sholl-Franco AJNi. Rod photoreceptor cell death is induced by okadaic acid through activation of PKC and L-type voltage-dependent Ca2+ channels and prevented by IGF-1 2010; 57(2): 128-35.
[66]
Rodriguez-de la Rosa, L; Fernandez-Sanchez, L; Germain, F; Murillo-Cuesta, S; Varela-Nieto, I; De La Villa, P P, et al. Age-related functional and structural retinal modifications in the Igf1−/− null mouse 2012; 46(2): 476-85.
[67]
Ruberte, J; Ayuso, E; Navarro, M; Carretero, A; Nacher, V; Haurigot, V Increased ocular levels of IGF-1 in transgenic mice lead to diabetes-like eye disease, 2004. 113(8)1149
[http://dx.doi.org/10.1172/JCI19478]
[68]
Kermer, P; Klöcker, N; Labes, M Bähr MJJoN., Insulin-like growth factor-I protects axotomized rat retinal ganglion cells from secondary death via PI3-K-dependent Akt phosphorylation and inhibition of caspase-3 in vivo 2000; 20(2): 722-8.
[69]
Yi, X.; Schubert, M.; Peachey, N.S. Insulin receptor substrate 2 is essential for maturation and survival of photoreceptor cells. J. Neurosci., 2005, 25(5), 1240-1248.
[http://dx.doi.org/10.1523/JNEUROSCI.3664-04.2005] [PMID: 15689562]
[70]
Chacón-Fernández, P; Säuberli, K; Colzani, M; Moreau, T; Ghevaert, C; Barde, Y-A Brain-derived neurotrophic factor in megakaryocytes., Journal of Biological Chemistry 2016. jbc. M116. 720029.
[http://dx.doi.org/10.1074/jbc.M116.720029]
[71]
Binder, D.K.; Scharfman, H.E. Brain-derived neurotrophic factor. Growth Factors, 2004, 22(3), 123-131.
[http://dx.doi.org/10.1080/08977190410001723308] [PMID: 15518235]
[72]
Hirsch, M.A.; van Wegen, E.E.H.; Newman, M.A.; Heyn, P.C. Exercise-induced increase in brain-derived neurotrophic factor in human Parkinson’s disease: a systematic review and meta-analysis. Transl. Neurodegener., 2018, 7(1), 7.
[http://dx.doi.org/10.1186/s40035-018-0112-1] [PMID: 29568518]
[73]
Castrén, E; Kojima, M Brain-derived neurotrophic factor in mood disorders and antidepressant treatments. , Neurobiol Dis 2017; 97(Pt 119-26.
[http://dx.doi.org/10.1016/j.nbd.2016.07.010] [PMID: 27425886]
[74]
Asai, N.; Abe, T.; Saito, T.; Sato, H.; Ishiguro, S.; Nishida, K. Temporal and spatial differences in expression of TrkB isoforms in rat retina during constant light exposure. Exp. Eye Res., 2007, 85(3), 346-355.
[http://dx.doi.org/10.1016/j.exer.2007.05.010] [PMID: 17640634]
[75]
Goldenberg-Cohen, N.; Avraham-Lubin, B-C.R.; Sadikov, T.; Askenasy, N. Effect of coadministration of neuronal growth factors on neuroglial differentiation of bone marrow-derived stem cells in the ischemic retina. Invest. Ophthalmol. Vis. Sci., 2014, 55(1), 502-512.
[http://dx.doi.org/10.1167/iovs.13-12223] [PMID: 24370836]
[76]
Harada, T.; Harada, C.; Nakayama, N. Modification of glial-neuronal cell interactions prevents photoreceptor apoptosis during light-induced retinal degeneration. Neuron, 2000, 26(2), 533-541.
[http://dx.doi.org/10.1016/S0896-6273(00)81185-X] [PMID: 10839371]
[77]
Kimura, A.; Namekata, K.; Guo, X.; Harada, C.; Harada, T. Neuroprotection, growth factors and BDNF-TrkB signalling in retinal degeneration. Int. J. Mol. Sci., 2016, 17(9), 1584.
[http://dx.doi.org/10.3390/ijms17091584] [PMID: 27657046]
[78]
Kong, L.; Zhou, X.; Li, F.; Yodoi, J.; McGinnis, J.; Cao, W. Neuroprotective effect of overexpression of thioredoxin on photoreceptor degeneration in Tubby mice. Neurobiol. Dis., 2010, 38(3), 446-455.
[http://dx.doi.org/10.1016/j.nbd.2010.03.005] [PMID: 20298786]
[79]
Bueker, E.D. Implantation of tumors in the hind limb field of the embryonic chick and the developmental response of the lumbosacral nervous system. Anat. Rec., 1948, 102(3), 369-389.
[http://dx.doi.org/10.1002/ar.1091020309] [PMID: 18098427]
[80]
Hefti, F. Pharmacology of nerve growth factor and discovery of tanezumab, an anti-nerve growth factor antibody and pain therapeutic. Pharmacol Res 2019.104240,
[http://dx.doi.org/10.1016/j.phrs.2019.04.024] [PMID: 31026504]
[81]
Garcia, T.B.; Hollborn, M.; Bringmann, A. Expression and signaling of NGF in the healthy and injured retina. Cytokine Growth Factor Rev., 2017, 34, 43-57.
[http://dx.doi.org/10.1016/j.cytogfr.2016.11.005] [PMID: 27964967]
[82]
Denk, F.; Bennett, D.L.; McMahon, S.B. Nerve growth factor and pain mechanisms. Annu. Rev. Neurosci., 2017, 40, 307-325.
[http://dx.doi.org/10.1146/annurev-neuro-072116-031121] [PMID: 28441116]
[83]
Skaper, S.D. Nerve growth factor: a neuroimmune crosstalk mediator for all seasons. Immunology, 2017, 151(1), 1-15.
[http://dx.doi.org/10.1111/imm.12717] [PMID: 28112808]
[84]
Tuszynski, M.H.; Yang, J.H.; Barba, D. Nerve growth factor gene therapy: activation of neuronal responses in Alzheimer disease. JAMA Neurol., 2015, 72(10), 1139-1147.
[http://dx.doi.org/10.1001/jamaneurol.2015.1807] [PMID: 26302439]
[85]
Chakrabarti, S.; Sima, A.A.; Lee, J.; Brachet, P.; Dicou, E. Nerve growth factor (NGF), proNGF and NGF receptor-like immunoreactivity in BB rat retina. Brain Res., 1990, 523(1), 11-15.
[http://dx.doi.org/10.1016/0006-8993(90)91630-Y] [PMID: 2169962]
[86]
Tirassa, P.; Rosso, P.; Iannitelli, A. Ocular nerve growth factor (ngf) and ngf eye drop application as paradigms to investigate ngf neuroprotective and reparative actions.neurotrophic factors: methods and protocols; New York, NY: Springer New York, 2018, pp. 19-38.
[http://dx.doi.org/10.1007/978-1-4939-7571-6_2]
[87]
Wang, J; Iacovelli, J; Spencer, C C, Saint-Geniez MJIo. science v Direct 148 effect of sodium iodate on neurosensory retina 2014; 55(3): 149 1941-53.
[88]
Sancho-Pelluz, J; Arango-Gonzalez, B; Kustermann, S; Romero, FJ; van Veen, T; Zrenner, E Photoreceptor cell death mechanisms in inherited retinal degeneration, 38(3): 253-69.
[http://dx.doi.org/10.1007/s12035-008-8045-9]
[89]
Lebrun-Julien, F; Bertrand, MJ; De Backer, O; Stellwagen, D; Morales, CR; Di Polo, A ProNGF induces TNFα-dependent death of retinal ganglion cells through a p75NTR non-cell-autonomous signaling pathway, 107(8): 3817-22.
[http://dx.doi.org/10.1073/pnas.0909276107]
[90]
Lambiase, A.; Mantelli, F.; Sacchetti, M.; Rossi, S.; Aloe, L.; Bonini, S. Clinical applications of NGF in ocular diseases. Arch. Ital. Biol., 2011, 149(2), 283-292.
[PMID: 21702001]
[91]
Lambiase, A.; Tirassa, P.; Micera, A.; Aloe, L.; Bonini, S. Pharmacokinetics of conjunctivally applied nerve growth factor in the retina and optic nerve of adult rats. Invest. Ophthalmol. Vis. Sci., 2005, 46(10), 3800-3806.
[http://dx.doi.org/10.1167/iovs.05-0301] [PMID: 16186366]
[92]
Sivilia, S.; Giuliani, A.; Fernández, M. Intravitreal NGF administration counteracts retina degeneration after permanent carotid artery occlusion in rat. BMC Neurosci., 2009, 10, 52.
[http://dx.doi.org/10.1186/1471-2202-10-52] [PMID: 19473529]
[93]
Carmignoto, G.; Maffei, L.; Candeo, P.; Canella, R.; Comelli, C. Effect of NGF on the survival of rat retinal ganglion cells following optic nerve section. J. Neurosci., 1989, 9(4), 1263-1272.
[http://dx.doi.org/10.1523/JNEUROSCI.09-04-01263.1989] [PMID: 2467970]
[94]
Lenzi, L.; Coassin, M.; Lambiase, A.; Bonini, S.; Amendola, T.; Aloe, L. Effect of exogenous administration of nerve growth factor in the retina of rats with inherited retinitis pigmentosa. Vision Res., 2005, 45(12), 1491-1500.
[http://dx.doi.org/10.1016/j.visres.2004.12.020] [PMID: 15781068]
[95]
Bonini, S.; Lambiase, A.; Rama, P. Phase ii randomized, double-masked, vehicle-controlled trial of recombinant human nerve growth factor for neurotrophic keratitis. Ophthalmology, 2018, 125(9), 1332-1343.
[http://dx.doi.org/10.1016/j.ophtha.2018.02.022] [PMID: 29653858]
[96]
Mellough, C.B.; Sernagor, E.; Moreno-Gimeno, I.; Steel, D.H.; Lako, M. Efficient stage-specific differentiation of human pluripotent stem cells toward retinal photoreceptor cells. Stem Cells, 2012, 30(4), 673-686.
[http://dx.doi.org/10.1002/stem.1037] [PMID: 22267304]
[97]
Huang, L.; Chen, M.; Zhang, W.; Sun, X.; Liu, B.; Ge, J. Retinoid acid and taurine promote NeuroD1-induced differentiation of induced pluripotent stem cells into retinal ganglion cells. Mol. Cell. Biochem., 2018, 438(1-2), 67-76.
[http://dx.doi.org/10.1007/s11010-017-3114-x] [PMID: 28766169]
[98]
Hu, Y.; Zhang, Y.; Tian, K.; Xun, C.; Wang, S.; Lv, D. Effects of nerve growth factor and basic fibroblast growth factor dual gene modification on rat bone marrow mesenchymal stem cell differentiation into neuron-like cells in vitro. Mol. Med. Rep., 2016, 13(1), 49-58.
[http://dx.doi.org/10.3892/mmr.2015.4553] [PMID: 26572749]
[99]
Jacquemin, E.; Jonet, L.; Oliver, L. Developmental regulation of acidic fibroblast growth factor (aFGF) expression in bovine retina. Int. J. Dev. Biol., 1993, 37(3), 417-423.
[PMID: 7507349]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy