Skip to main content
Top
Published in: BMC Ophthalmology 1/2019

Open Access 01-12-2019 | Research article

Therapeutic effect of vasoactive intestinal peptide on form-deprived amblyopic kittens

Authors: Bo Li, Yunchun Zou, Liwen Li, Hongwei Deng, Wei Mi, Xing Wang, Ximin Yin

Published in: BMC Ophthalmology | Issue 1/2019

Login to get access

Abstract

Background

Exploring the role of vasoactive intestinal peptide (VIP) in the lateral geniculate body (LGBd) in visual development and studying the therapeutic effect of VIP on amblyopic kittens.

Methods

Three-week-old domestic cats were divided into a control group (n = 10) and a monocular deprivation group (n = 20), with an eye mask covering the right eye of those in the deprived group. After pattern visual evoked potential (PVEP) recording confirmed the formation of monocular amblyopia, the left LGBd was isolated from 5 kittens in each group. The remaining control kittens continued to be raised, and the remaining deprivation group was divided into a VIP intervention group (n = 5), Sefsol (caprylic acid monoglyceride, VIP solution) intervention group (n = 5) and amblyopia non-intervention group (n = 5) after removal of the eye mask. Three weeks later, PVEPs, VIP immunohistochemistry and VIP mRNA expression in the left LGBd were compared across groups.

Results

At 6 weeks of age, there were significant differences in P100 wave latency and amplitude and VIP immunohistochemistry and in situ hybridization between the control group and the deprivation group (P < 0.05). After 3 weeks of the corresponding interventions, the latency and amplitude in the VIP intervention group were better than that in the Sefsol intervention group and amblyopia non-intervention group (P < 0.05). Furthermore, VIP treatment increased the number of immunohistochemical VIP-positive cells (P < 0.05) and the average optical density of positive cells (P > 0.05), as well as the number (P < 0.05) and average optical density of VIP mRNA-positive cells (P < 0.05).

Conclusions

VIP plays an important role in visual development. Nasal administration of VIP can improve the function of neurons in the LGBd of kittens and has a certain therapeutic effect on amblyopia.
Literature
1.
go back to reference Von Noorden GK. Histological studies of the visual system in monkeys with experimental amblyopia. Investig Ophthalmol. 1973;12:727–38. Von Noorden GK. Histological studies of the visual system in monkeys with experimental amblyopia. Investig Ophthalmol. 1973;12:727–38.
2.
go back to reference Piscopo DM, El-Danaf RN, Huberman AD, Niell CM. Diverse visual features encoded in mouse lateral geniculate nucleus. J Neurosci. 2013;33:4642–56.CrossRef Piscopo DM, El-Danaf RN, Huberman AD, Niell CM. Diverse visual features encoded in mouse lateral geniculate nucleus. J Neurosci. 2013;33:4642–56.CrossRef
3.
go back to reference Wiesel TN, Hubel DH. Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. J Neurophysiol. 1963;26:978–93.CrossRef Wiesel TN, Hubel DH. Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. J Neurophysiol. 1963;26:978–93.CrossRef
4.
go back to reference Guillery RW, Stelzner DJ. The differential effects of unilateral lid closure upon the monocular and binocular segments of the dorsal lateral geniculate nucleus in the cat. J Comp Neurol. 1970;139:413–21.CrossRef Guillery RW, Stelzner DJ. The differential effects of unilateral lid closure upon the monocular and binocular segments of the dorsal lateral geniculate nucleus in the cat. J Comp Neurol. 1970;139:413–21.CrossRef
5.
go back to reference Takahata T, Patel NB, Balaram P, Chino YM, Kaas JH. Long-term histological changes in the macaque primary visual cortex and the lateral geniculate nucleus after monocular deprivation produced by early restricted retinal lesions and diffuser induced form deprivation. J Comp Neurol. 2018;526:2955–72.CrossRef Takahata T, Patel NB, Balaram P, Chino YM, Kaas JH. Long-term histological changes in the macaque primary visual cortex and the lateral geniculate nucleus after monocular deprivation produced by early restricted retinal lesions and diffuser induced form deprivation. J Comp Neurol. 2018;526:2955–72.CrossRef
6.
go back to reference Toporova SN, Alekseenko SV, Makarov FN. Afferent connections of fields 17 and 18 of the cat cerebral cortex formed by neurons of the dorsal lateral geniculate body. Neurosci Behav Physiol. 2004;34:515–8.CrossRef Toporova SN, Alekseenko SV, Makarov FN. Afferent connections of fields 17 and 18 of the cat cerebral cortex formed by neurons of the dorsal lateral geniculate body. Neurosci Behav Physiol. 2004;34:515–8.CrossRef
7.
go back to reference Jaepel J, Hubener M, Bonhoeffer T, Rose T. Lateral geniculate neurons projecting to primary visual cortex show ocular dominance plasticity in adult mice. Nat Neurosci. 2017;20:1708–14.CrossRef Jaepel J, Hubener M, Bonhoeffer T, Rose T. Lateral geniculate neurons projecting to primary visual cortex show ocular dominance plasticity in adult mice. Nat Neurosci. 2017;20:1708–14.CrossRef
8.
go back to reference Said SI, Rosenberg RN. Vasoactive intestinal polypeptide: abundant immunoreactivity in neural cell lines and normal nervous tissue. Science. 1976;192:907–8.CrossRef Said SI, Rosenberg RN. Vasoactive intestinal polypeptide: abundant immunoreactivity in neural cell lines and normal nervous tissue. Science. 1976;192:907–8.CrossRef
9.
go back to reference Fuxe K, Hökfelt T, Said SI, Mutt V. Vasoactive intestinal polypeptide and the nervous system: immunohistochemical evidence for localization in central and peripheral neurons, particularly intracortical neurons of the cerebral cortex. Neurosci Lett. 1977;5:241–6.CrossRef Fuxe K, Hökfelt T, Said SI, Mutt V. Vasoactive intestinal polypeptide and the nervous system: immunohistochemical evidence for localization in central and peripheral neurons, particularly intracortical neurons of the cerebral cortex. Neurosci Lett. 1977;5:241–6.CrossRef
10.
go back to reference Lorén I, Emson PC, Fahrenkrug J, Björklund A, Alumets J, Håkanson R, et al. Distribution of vasoactive intestinal polypeptide in the rat and mouse brain. Neuroscience. 1979;4:1953–76.CrossRef Lorén I, Emson PC, Fahrenkrug J, Björklund A, Alumets J, Håkanson R, et al. Distribution of vasoactive intestinal polypeptide in the rat and mouse brain. Neuroscience. 1979;4:1953–76.CrossRef
11.
go back to reference Uddman R, Alumets J, Ehinger B, Hakanson R, Loren I, Sundler F. Vasoactive intestinal peptide nerves in ocular and orbital structures of the cat. Invest Ophthalmol Vis Sci. 1980;19:878–85.PubMed Uddman R, Alumets J, Ehinger B, Hakanson R, Loren I, Sundler F. Vasoactive intestinal peptide nerves in ocular and orbital structures of the cat. Invest Ophthalmol Vis Sci. 1980;19:878–85.PubMed
12.
go back to reference Emson PC, Gilbert RF, Loren I, Fahrenkrug J, Sundler F, Schaffalitzky de Muckadell OB. Development of vasoactive intestinal polypeptide (VIP) containing neurones in the rat brain. Brain Res. 1979;177:437–44.CrossRef Emson PC, Gilbert RF, Loren I, Fahrenkrug J, Sundler F, Schaffalitzky de Muckadell OB. Development of vasoactive intestinal polypeptide (VIP) containing neurones in the rat brain. Brain Res. 1979;177:437–44.CrossRef
13.
go back to reference Cakmak AI, Basmak H, Gursoy H, Ozkurt M, Yildirim N, Erkasap N, et al. Vasoactive intestinal peptide, a promising agent for myopia? Int J Ophthalmol. 2017;10:211–6.PubMedPubMedCentral Cakmak AI, Basmak H, Gursoy H, Ozkurt M, Yildirim N, Erkasap N, et al. Vasoactive intestinal peptide, a promising agent for myopia? Int J Ophthalmol. 2017;10:211–6.PubMedPubMedCentral
14.
go back to reference Ogawa-Meguro R, Itoh K, Mizuno N. Substance P-, vasoactive intestinal polypeptide-, and cholecystokinin-like immunoreactive fiber projections from the superior colliculus to the dorsal lateral geniculate nucleus in the rat. Exp Brain Res. 1992;89:59–66.CrossRef Ogawa-Meguro R, Itoh K, Mizuno N. Substance P-, vasoactive intestinal polypeptide-, and cholecystokinin-like immunoreactive fiber projections from the superior colliculus to the dorsal lateral geniculate nucleus in the rat. Exp Brain Res. 1992;89:59–66.CrossRef
15.
go back to reference Rittenhouse CD, Shouval HZ, Paradiso MA, Bear MF. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature. 1999;397:347–50.CrossRef Rittenhouse CD, Shouval HZ, Paradiso MA, Bear MF. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature. 1999;397:347–50.CrossRef
16.
go back to reference Bryant MG, Polak MM, Modlin I, Bloom SR, Albuquerque RH, Pearse AG. Possible dual role for vasoactive intestinal peptide as gastrointestinal hormone and neurotransmitter substance. Lancet. 1976;1:991–3.CrossRef Bryant MG, Polak MM, Modlin I, Bloom SR, Albuquerque RH, Pearse AG. Possible dual role for vasoactive intestinal peptide as gastrointestinal hormone and neurotransmitter substance. Lancet. 1976;1:991–3.CrossRef
17.
go back to reference Quik M, Iversen LL, Bloom SR. Effect of vasoactive intestinal peptide (VIP) and other peptides on cAMP accumulation in rat brain. Biochem Pharmacol. 1978;27:2209–13.CrossRef Quik M, Iversen LL, Bloom SR. Effect of vasoactive intestinal peptide (VIP) and other peptides on cAMP accumulation in rat brain. Biochem Pharmacol. 1978;27:2209–13.CrossRef
18.
go back to reference Ishihara T, Shigemoto R, Mori K, Takahashi K, Nagata S. Functional expression and tissue distribution of a novel receptor for vasoactive intestinal polypeptide. Neuron. 1992;8:811–9.CrossRef Ishihara T, Shigemoto R, Mori K, Takahashi K, Nagata S. Functional expression and tissue distribution of a novel receptor for vasoactive intestinal polypeptide. Neuron. 1992;8:811–9.CrossRef
19.
go back to reference Dejda A, Sokolowska P, Nowak JZ. Neuroprotective potential of three neuropeptides PACAP. VIP and PHI Pharmacol Rep. 2005;57:307–20.PubMed Dejda A, Sokolowska P, Nowak JZ. Neuroprotective potential of three neuropeptides PACAP. VIP and PHI Pharmacol Rep. 2005;57:307–20.PubMed
20.
go back to reference Vosko A, van Diepen HC, Kuljis D, Chiu AM, Heyer D, Terra H, et al. Role of vasoactive intestinal peptide in the light input to the circadian system. Eur J Neurosci. 2015;42:1839–48.CrossRef Vosko A, van Diepen HC, Kuljis D, Chiu AM, Heyer D, Terra H, et al. Role of vasoactive intestinal peptide in the light input to the circadian system. Eur J Neurosci. 2015;42:1839–48.CrossRef
21.
go back to reference Hermanstyne TO, Simms CL, Carrasquillo Y, Herzog ED, Nerbonne JM. Distinct firing properties of vasoactive intestinal peptide-expressing neurons in the suprachiasmatic nucleus. J Biol Rhythm. 2016;31:57–67.CrossRef Hermanstyne TO, Simms CL, Carrasquillo Y, Herzog ED, Nerbonne JM. Distinct firing properties of vasoactive intestinal peptide-expressing neurons in the suprachiasmatic nucleus. J Biol Rhythm. 2016;31:57–67.CrossRef
22.
go back to reference Kudo T, Tahara Y, Gamble KL, McMahon DG, Block GD, Colwell CS. Vasoactive intestinal peptide produces long-lasting changes in neural activity in the suprachiasmatic nucleus. J Neurophysiol. 2013;110:1097–106.CrossRef Kudo T, Tahara Y, Gamble KL, McMahon DG, Block GD, Colwell CS. Vasoactive intestinal peptide produces long-lasting changes in neural activity in the suprachiasmatic nucleus. J Neurophysiol. 2013;110:1097–106.CrossRef
23.
go back to reference Brenneman DE, Eiden LE. Vasoactive intestinal peptide and electrical activity influence neuronal survival. Proc Natl Acad Sci U S A. 1986;83:1159–62.CrossRef Brenneman DE, Eiden LE. Vasoactive intestinal peptide and electrical activity influence neuronal survival. Proc Natl Acad Sci U S A. 1986;83:1159–62.CrossRef
24.
go back to reference Antonawich FJ, Said SI. Vasoactive intestinal peptide attenuates cytochrome c translocation, and apoptosis, in rat hippocampal stem cells. Neurosci Lett. 2002;325:151–4.CrossRef Antonawich FJ, Said SI. Vasoactive intestinal peptide attenuates cytochrome c translocation, and apoptosis, in rat hippocampal stem cells. Neurosci Lett. 2002;325:151–4.CrossRef
25.
go back to reference Delgado M, Ganea D. Vasoactive intestinal peptide prevents activated microglia-induced neurodegeneration under inflammatory conditions: potential therapeutic role in brain trauma. FASEB J. 2003;17:1922–4.CrossRef Delgado M, Ganea D. Vasoactive intestinal peptide prevents activated microglia-induced neurodegeneration under inflammatory conditions: potential therapeutic role in brain trauma. FASEB J. 2003;17:1922–4.CrossRef
26.
go back to reference Tan YV, Waschek JA, Targeting VIP. PACAP receptor signalling: new therapeutic strategies in multiple sclerosis. ASN Neuro. 2011;3:e65.CrossRef Tan YV, Waschek JA, Targeting VIP. PACAP receptor signalling: new therapeutic strategies in multiple sclerosis. ASN Neuro. 2011;3:e65.CrossRef
27.
go back to reference Brenneman DE, Neale EA, Foster GA, d'Autremont SW, Westbrook GL. Nonneuronal cells mediate neurotrophic action of vasoactive intestinal peptide. J Cell Biol. 1987;104:1603–10.CrossRef Brenneman DE, Neale EA, Foster GA, d'Autremont SW, Westbrook GL. Nonneuronal cells mediate neurotrophic action of vasoactive intestinal peptide. J Cell Biol. 1987;104:1603–10.CrossRef
28.
go back to reference Pincus DW, DiCicco-Bloom E, Black IB. Trophic mechanisms regulate mitotic neuronal precursors: role of vasoactive intestinal peptide (VIP). Brain Res. 1994;663:51–60.CrossRef Pincus DW, DiCicco-Bloom E, Black IB. Trophic mechanisms regulate mitotic neuronal precursors: role of vasoactive intestinal peptide (VIP). Brain Res. 1994;663:51–60.CrossRef
29.
go back to reference Magistretti PJ, Morrison JH, Shoemaker WJ, Sapin V, Bloom FE. Vasoactive intestinal polypeptide induces glycogenolysis in mouse cortical slices: a possible regulatory mechanism for the local control of energy metabolism. Proc Natl Acad Sci U S A. 1981;78:6535–9.CrossRef Magistretti PJ, Morrison JH, Shoemaker WJ, Sapin V, Bloom FE. Vasoactive intestinal polypeptide induces glycogenolysis in mouse cortical slices: a possible regulatory mechanism for the local control of energy metabolism. Proc Natl Acad Sci U S A. 1981;78:6535–9.CrossRef
30.
go back to reference Vu JP, Larauche M, Flores M, Luong L, Norris J, Oh S, et al. Regulation of appetite, body composition, and metabolic hormones by vasoactive intestinal polypeptide (VIP). J Mol Neurosci. 2015;56:377–87.CrossRef Vu JP, Larauche M, Flores M, Luong L, Norris J, Oh S, et al. Regulation of appetite, body composition, and metabolic hormones by vasoactive intestinal polypeptide (VIP). J Mol Neurosci. 2015;56:377–87.CrossRef
31.
go back to reference Arden GB, Barnard WM, Mushin AS. Visually evoked responses in amblyopia. Br J Ophthalmol. 1974;58:183–92.CrossRef Arden GB, Barnard WM, Mushin AS. Visually evoked responses in amblyopia. Br J Ophthalmol. 1974;58:183–92.CrossRef
32.
go back to reference Snyder A, Shapley R. Deficits in the visual evoked potentials of cats as a result of visual deprivation. Exp Brain Res. 1979;37:73–86.CrossRef Snyder A, Shapley R. Deficits in the visual evoked potentials of cats as a result of visual deprivation. Exp Brain Res. 1979;37:73–86.CrossRef
33.
go back to reference Jang J, Kyung SE. Assessing amblyopia treatment using multifocal visual evoked potentials. BMC Ophthalmol. 2018;18:196.CrossRef Jang J, Kyung SE. Assessing amblyopia treatment using multifocal visual evoked potentials. BMC Ophthalmol. 2018;18:196.CrossRef
34.
go back to reference Hubel DH, Wiesel TN. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol. 1970;206:419–36.CrossRef Hubel DH, Wiesel TN. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol. 1970;206:419–36.CrossRef
35.
go back to reference Duffy KR, Lingley AJ, Holman KD, Mitchell DE. Susceptibility to monocular deprivation following immersion in darkness either late into or beyond the critical period. J Comp Neurol. 2016;524:2643–53.CrossRef Duffy KR, Lingley AJ, Holman KD, Mitchell DE. Susceptibility to monocular deprivation following immersion in darkness either late into or beyond the critical period. J Comp Neurol. 2016;524:2643–53.CrossRef
36.
go back to reference Montey KL, Quinlan EM. Recovery from chronic monocular deprivation following reactivation of thalamocortical plasticity by dark exposure. Nat Commun. 2011;2:317.CrossRef Montey KL, Quinlan EM. Recovery from chronic monocular deprivation following reactivation of thalamocortical plasticity by dark exposure. Nat Commun. 2011;2:317.CrossRef
37.
go back to reference Mitchell DE, MacNeill K, Crowder NA, Holman K, Duffy KR. Recovery of visual functions in amblyopic animals following brief exposure to total darkness. J Physiol. 2016;594:149–67.CrossRef Mitchell DE, MacNeill K, Crowder NA, Holman K, Duffy KR. Recovery of visual functions in amblyopic animals following brief exposure to total darkness. J Physiol. 2016;594:149–67.CrossRef
38.
go back to reference Suzuki M, Nagae M, Nagata Y, Kumagai N, Inui K, Kakigi R. Effects of refractive errors on visual evoked magnetic fields. BMC Ophthalmol. 2015;15:162.CrossRef Suzuki M, Nagae M, Nagata Y, Kumagai N, Inui K, Kakigi R. Effects of refractive errors on visual evoked magnetic fields. BMC Ophthalmol. 2015;15:162.CrossRef
39.
go back to reference Gozes I, Bardea A, Reshef A, Zamostiano R, Zhukovsky S, Rubinraut S, et al. Neuroprotective strategy for Alzheimer disease: intranasal administration of a fatty neuropeptide. Proc Natl Acad Sci U S A. 1996;93:427–32.CrossRef Gozes I, Bardea A, Reshef A, Zamostiano R, Zhukovsky S, Rubinraut S, et al. Neuroprotective strategy for Alzheimer disease: intranasal administration of a fatty neuropeptide. Proc Natl Acad Sci U S A. 1996;93:427–32.CrossRef
40.
go back to reference Dufes C, Olivier JC, Gaillard F, Gaillard A, Couet W, Muller JM. Brain delivery of vasoactive intestinal peptide (VIP) following nasal administration to rats. Int J Pharm. 2003;255:87–97.CrossRef Dufes C, Olivier JC, Gaillard F, Gaillard A, Couet W, Muller JM. Brain delivery of vasoactive intestinal peptide (VIP) following nasal administration to rats. Int J Pharm. 2003;255:87–97.CrossRef
41.
go back to reference Duffy KR, Fong MF, Mitchell DE, Bear MF. Recovery from the anatomical effects of long-term monocular deprivation in cat lateral geniculate nucleus. J Comp Neurol. 2018;526:310–23.CrossRef Duffy KR, Fong MF, Mitchell DE, Bear MF. Recovery from the anatomical effects of long-term monocular deprivation in cat lateral geniculate nucleus. J Comp Neurol. 2018;526:310–23.CrossRef
Metadata
Title
Therapeutic effect of vasoactive intestinal peptide on form-deprived amblyopic kittens
Authors
Bo Li
Yunchun Zou
Liwen Li
Hongwei Deng
Wei Mi
Xing Wang
Ximin Yin
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Ophthalmology / Issue 1/2019
Electronic ISSN: 1471-2415
DOI
https://doi.org/10.1186/s12886-019-1203-1

Other articles of this Issue 1/2019

BMC Ophthalmology 1/2019 Go to the issue