Morphology and neurochemistry of rabbit iris innervation

Experimental Eye Research

Volumn 135, Issue , 2015, Pages 182-191

  He, Jiucheng ^a   Bazan, Haydee E P ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Anterior uveitis; Calcitonin gene related peptide; Iris innervation; Neurogenic inflammation; Neuropeptides; Sensory nerves; Substance P; Trigeminal ganglia

Indexed keywords

BETA TUBULIN; CALCITONIN GENE RELATED PEPTIDE; NEUROPEPTIDE; SUBSTANCE P;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATARACT; COMPUTER ANALYSIS; CONTROLLED STUDY; EXPERIMENTAL RABBIT; EYE PAIN; FEMALE; GLAUCOMA; INNERVATION; IRIDOCYCLITIS; IRIS; MALE; MORPHOLOGY; NERVE CELL; NERVE FIBER; NERVE PLEXUS; NEUROCHEMISTRY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUPIL; STROMA; TRIGEMINAL NERVE; TRIGEMINUS GANGLION; ANATOMY AND HISTOLOGY; ANIMAL; CHEMISTRY; CYTOLOGY; PHYSIOLOGY; RABBIT;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; IRIS; NERVE FIBERS; NEUROPEPTIDES; PUPIL; RABBITS; SUBSTANCE P; TRIGEMINAL GANGLION;

EID: 84937978451     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2015.03.005     Document Type: Article

References (52)

1. Ayer-Le Lievre C.S., Granholm A.C., Sieger A. Silver impregnation of intrinsic sensory innervation of rat iris in toto. J.Anat. 1984, 138:309-321.
2. Bae S.J., Matsunaga Y., Takenaka M., Tanaka Y., Hamazaki Y., Shimizu K., Katayama I. Substance P induced preprotachykinin-α mRNA, neutral endopeptidase mRNA and substance P in cultured normal fibroblasts. Int. Arch. Allergy Immunol. 2002, 127:316-321.
3. Beckers H.J., Klooster J., Vrensen G.F., Lamers W.P. Substance P in rat corneal and iridal nerves: an ultrastructural immunohistochemical study. Ophthalmic Res. 1993, 25:192-200.
4. Brain S.D., Williams T.J., Tippins J.R., Morris H.R. MacIntyre I. Calcitonin gene-related peptide is a potent vasodilator. Nature 1985, 313:54-56.
5. Cortina M.S., He J., Li N., Bazan N.G., Bazan H.E.P. Neuroprotectin D1 synthesis and corneal nerve regeneration after experimental surgery and treatment with PEDF plus DHA. Investig. Ophthalmol. Vis. Sci. 2010, 51:804-810.
6. Cortina M.S., He J., Li N., Bazan N.G., Bazan H.E.P. Recovery of corneal sensitivity, CGRP positive nerves and increased wound healing are induced by PEDF plus DHA after experimental surgery. Arch. Ophthalmol. 2012, 130:76-83.
7. Cortina M.S., He J., Russ T., Bazan N.G., Bazan H.E.P. Neuroprotectin D1 (NPD1) restores corneal nerve integrity and function after damage from experimental surgery. Investig. Ophthalmol. Vis. Sci. 2013, 54:4109-4116.
8. De Felipe C., Herrero J.F., O'Brien J.A., Palmer J.A., Doyle C.A., Smith A.J., Laird J.M., Belmonte C., Cervero F., Hunt S.P. Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature 1998, 392:394-397.
9. Donkin J.J., Turner R.J., Hassan I., Vink R. Substance P in traumatic brain injury. Prog. Brain Res. 2007, 161:97-109.
10. Durham P.L. Calcitonin gene-related peptide and migraine. Headache 2006, 46:S3-S8.
11. Edvinsson L., Ho T.W. CGRP receptor antagonism and migraine. Neurotherapeutics 2010, 7:164-175.
12. Eftekhari S., Edvinsson L. Possible sites of action of the new calcitonin gene-related peptide receptor antagonists. Ther. Adv. Neurol. Disord. 2010, 3:369-378.
13. Ehinger B. Double innervation of the feline iris dilator. Arch. Ophthalmol. 1967, 77:541-545.
14. Esquenazi S., Bazan H.E.P., Bui V., He J., Kim D.B., Bazan N.G. Topical combination of NGF and DHA increases rabbit corneal generation after PRK. Investig. Ophthalmol. Vis. Sci. 2005, 46:3121-3127.
15. Fujimara M., Hayashi H., Muramatsu I., Ueda N. Supersensitivity of the rabbit iris sphincter muscle induced by trigeminal denervation: the role of substance P. J.Physiol. 1984, 350:583-597.
16. Fujishima H., Takeyama M., Takeuchi T., Saito I., Tsubota K. Elevated levels of substance P in tears of patients with allergic conjunctivitis and vernal keratoconjunctivitis. Clin. Exp. Allergy 1997, 27:372-378.
17. Gibbins I.L., Morris J.L. Co-existence of neuropeptides in sympathetic, cranial autonomic and sensory neurons innervating the iris of the guinea-pig. J.Auton. Nerv. Syst. 1987, 21:67-82.
18. He J., Bazan N.G., Bazan H.E. Mapping the entire human corneal nerve architecture. Exp. Eye Res. 2010, 91:513-523.
19. He J., Bazan H.E. Mapping the nerve architecture of diabetic human corneas. Ophthalmology 2012, 119:956-964.
20. He J., Bazan H.E. Corneal nerve architecture in a donor with unilateral corneal epithelial basement membrane dystrophy. Ophthalmic Res. 2013, 49:185-191.
21. Hirai R., Tamamaki N., Hukami K., Nojyo Y. Ultrastructural analysis of tyrosine hydroxylase-, substance P-, and calcitonin gene-related peptide-immunoreactive nerve fibers in the rat iris. Ophthalmic Res. 1994, 26:169-180.
22. Ivanusic J.J., Wood R.J., Brock J.A. Sensory and sympathetic innervation of the mouse and guinea pig corneal epithelium. J.Comp. Neurol. 2013, 521:877-893.
23. Jones M.A., Marfurt C.F. Peptidergic innervation of the rat cornea. Exp. Eye Res. 1998, 66:421-435.
24. Jones S., Tucker K.L., Sage T., Kaiser W.J., Barrett N.E., Lowry P.J., Zimmer A., Hunt S.P., Emerson M., Gibbins J.M. Peripheral tachykinins and the neurokinin receptor NK1 are required for platelet thrombus formation. Blood 2008, 111:605-612.
25. Ko J.A., Mizuno Y., Ohki C., Chikama T., Sonoda K.H., Kiuchi Y. Neuropeptides released trigeminal neurons promote the stratification of human corneal epithelial cells. Investig. Ophthalmol. Vis. Sci. 2014, 55:125-133.
26. Krootila K. CGRP inrelation to neurogenic inflammation and cAMP in the rabbit eye. Exp. Eye Res. 1988, 47:307-316.
27. Krootila K., Uusitalo H., Palkama A. Effect of neurogenic irritation and calcitonin gene-related peptide (CGRP) on ocular blood flow in the rabbit. Curr. Eye Res. 1988, 7:695-703.
28. Kuwayama Y., Stone R.A. Distinct substance P and calcitonin gene-related peptide immunoreactive nerves in the guinea pig eye. Investig. Ophthalmol. Vis. Sci. 1987, 28:1947-1954.
29. Lai J.P., Douglas S.D., Ho W.Z. Human lymphocytes express substance P and its receptor. J.Neuroimmunol. 1998, 86:80-86.
30. Lambiase A., Bonini S., Micera A., Tirassa P., Magrini L., Bonini S., Aloe L. Increased plasma levels of substance P in vernal keratoconjunctivitis. Investig. Ophthalmol. Vis. Sci. 1997, 38:2161-2164.
31. Lee Y., Kawai Y., Shiosaka S., Takami K., Kiyama H., Hillyard C.J., Girgis S., MacIntyre I., Emson P.C., Tohyama M. Coexistence of calcitonin gene-related peptide and substance P-like peptide in single cells of the trigeminal ganglion of the rat: immunohistochemical analysis. Brain Res. 1985, 330:194-196.
32. Linnik M.D., Moscowitz M.A. Identification of immunoreactive substance P in human and other mammalian endothelial cells. Peptides 1989, 10:957-962.
33. McCulloch J., Uddman R., Kingman T.A., Edvinsson L. Calcitonin gene-related peptide: functional role in cerebrovascular regulation. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:5731-5735.
34. Motterle L., Diebold Y., Enríquez de Salamanca A., Saez V., Garcia-Vazquez C., Stern M.E., Calonge M., Leonardi A. Altered expression of neurotransmitter receptors and neuromediators in vernal keratoconjunctivitis. Arch. Ophthalmol. 2006, 124:462-468.
35. Neuhuber W., Schrodl F. Autonomic control of the eye and the iris. Auton. Neurosci. 2011, 165:67-79.
36. Nishida T., Nakamura M., Ofuji K., Reid T.W., Mannis M.J., Murphy C.J. Synergistic effects of substance P with insulin-like growth factor-1 on epithelial migration of the cornea. J.Cell. Physiol. 1996, 169:159-166.
37. Reid T.W., Murphy C.J., Iwahashi C.K., Foster B.A., Mannis M.J. Stimulation of epithelial cell growth by the neuropeptide substance P. J.Cell Biochem. 1993, 52:476-485.
38. Rodriguse M.M., Hackett J., Donohoo P. Iris. Ocular Anatomy, Embryology, and Teratology. Chapter 9 1982, 285-302. Harper & Row. first ed. F.A. Jakobiec (Ed.).
39. Rosenblatt M.I., Dahl G.P., Dickerson I.M. Characterization and localization of the rabbit ocular calcitonin generelated peptide (CGRP)-receptor component protein (RCP). Investig. Ophthalmol. Vis. Sci. 2000, 41:1159-1167.
40. Rosenfeld M.G., Mermod J.J., Amara S.G., Swanson L.W., Sawchenko P.E., Rivier J., Vale W.W., Evans R.M. Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature 1983, 304:129-135.
41. Seiger A., Selin U.B., Kessler J., Black I., Ayer-Lelievre C. Substance P-containing sensory nerves in the rat iris. Normal distribution, ontogeny and innervation of intraocular iris grafts. Neuroscience 1985, 15:519-528.
42. Selbach J.M., Gottanka J., Wittmann M., Lütjen-Drecoll E. Efferent and afferent innervation of primate trabecular meshwork and scleral spur. Investig. Ophthalmol. Vis. Sci. 2000, 41:2184-2191.
43. Skofitsch G., Jacobowitz D.M. Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat. Peptides 1985, 6:747-754.
44. Stone R.A., Laties A.M., Brecha N.C. Substance P-like immunoreactive nerves in the anterior segment of the rabbit, cat and monkey eye. Neuroscience 1982, 7:2459-2468.
45. Taylor A.W., Yee D.G., Streilein J.W. Suppression of nitric oxide generated by inflammatory microphages by calcitonin gene-related peptide in aqueous humor. Investig. Ophthalmol. Vis. Sci. 1998, 39:1372-1378.
46. Terenghi G., Polak J.M., Ghatei M.A., Mulderry P.K., Butler J.M., Unger W.G., Bloom S.R. Distribution and origin of calcitonin gene-related peptide (CGRP) immunoreactivity in the sensory innervation of the mammalian eye. J.Comp. Neurol. 1985, 233:506-516.
47. Tervo K., Tervo T., Eränkö L., Eränkö O., Cuello A.C. Immunoreactivity for substance P in the Gasserion ganglion, ophthalmic nerve and anterior segment of the rabbit eye. Histochem. J. 1981, 13:435-443.
48. Troger J., Kremser B., Stockl T., Kralinger M., Schimid E., Kunze C., Kiseselbach G.F. Elevated levels of calcitonin gene-related peptide in aqueous humor of patients with proliferative vitreoretinopathy. Greafe's Arch. Clin. Exp. Ophthalmol. 2000, 238:237-242.
49. Ueda N., Muramatsu I., Hayashi H., Fujiwara M. Trigeminal nerve: possible origin of substance P-nergic response in isolated rabbit iris sphincter muscle. Life Sci. 1982, 31:369-375.
50. Unger W.G., Terenghi G., Ghatei M.A., Ennis K.W., Butler J.M., Zhang S.Q., Too H.P., Polak J.M., Bloom S.R. Calcitonin gene-related polypeptide as a mediator of the neurogenic ocular injury response. J.Ocul. Pharmacol. 1985, 1:189-199.
51. Wahlestedt C., Beding B., Ekman R., Oksala O., Stjernschantz J., Håkanson R. Calcitonin gene-related peptide in the eye: release by sensory nerve stimulation and effects associated with neurogenic inflammation. Regul. Pept. 1986, 16:107-115.
52. Zubrzycka M., Janecka A. Substance P: transmitter of nociception (Minireview). Endocr. Regul. 2000, 34:195-201.