#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Histological and immunohistochemical characterization of the porcine ocular surface


Autoři: Mario Crespo-Moral aff001;  Laura García-Posadas aff001;  Antonio López-García aff001;  Yolanda Diebold aff001
Působiště autorů: Ocular Surface Group, IOBA – University of Valladolid, Valladolid, Spain aff001;  Biomedical Research Networking Center on Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Valladolid, Spain aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227732

Souhrn

The ocular surface of the white domestic pig (Sus scrofa domestica) is used as a helpful model of the human ocular surface; however, a complete histological description has yet to be published. In this work, we studied porcine eyeballs with intact eyelids to describe and characterize the different structures that form the ocular surface, including the cornea and conjunctiva that covers the bulbar sclera, tarsi, and the nictitating membrane. We determined the distribution of goblet cells of different types over the conjunctiva and analyzed the conjunctival-associated lymphoid tissue (CALT). Porcine eyeballs were obtained from a local slaughterhouse, fixed, processed, and embedded in paraffin blocks. Tissue sections (4 μm) were stained with hematoxylin/eosin, Alcian blue/Periodic Acid Schiff, and Giemsa. Slides were also stained with lectins from Arachis hypogaea (PNA) and Helix pomatia (HPA) agglutinins and immunostained with rabbit anti-CD3. We found that the porcine cornea was composed of 6–8 epithelial cell layers, stroma, Descemet’s membrane, and an endothelial monolayer. The total corneal thickness was 1131.0±87.5 μm (mean±standard error of the mean) in the center and increased to 1496.9±138.2 μm at the limbus. The goblet cell density was 71.25±12.29 cells/mm, ranging from the highest density (113.04±37.21 cells/mm) in the lower palpebral conjunctiva to the lowest density (12.69±4.29 cells/mm) in the bulbar conjunctiva. The CALT was distributed in the form of intraepithelial lymphocytes and subepithelial diffuse lymphoid tissue. Lenticular-shaped lymphoid follicles, about 8 per histological section, were also present within the conjunctival areas. In conclusion, we demonstrated that the analyzed porcine ocular structures are similar to those of humans, confirming the potential usefulness of pig eyes to study ocular surface physiology and pathophysiology.

Klíčová slova:

Animal ocular anatomy – Cornea – Epithelium – Eyelids – Eyes – Pig models – Swine – Lymphoid tissue


Zdroje

1. Fine BS, Yanoff M. Ocular Histology. Second. Hagerstown, Maryland: Harper & Row Publishers; 1979.

2. Stern ME, Beuerman RW, Fox RI, Gao J, Mircheff AK, Pflugfelder SC. The pathology of dry eye: The interaction between the ocular surface and lacrimal glands. Cornea. 1998. doi: 10.1097/00003226-199811000-00002 9820935

3. Schlötzer-Schrehardt U, Kruse FE. Identification and characterization of limbal stem cells. Exp Eye Res. 2005. doi: 10.1016/j.exer.2005.02.016 16051216

4. Hodges RR, Dartt DA. Tear film mucins: Front line defenders of the ocular surface; comparison with airway and gastrointestinal tract mucins. Exp Eye Res. 2013. doi: 10.1016/j.exer.2013.07.027 23954166

5. Dartt DA. Control of mucin production by ocular surface epithelial cells. Exp Eye Res. 2004. pp. 173–185. doi: 10.1016/j.exer.2003.10.005 14729350

6. Dartt D a, Masli S. Conjunctival epithelial and goblet cell function in chronic inflammation and ocular allergic inflammation. Curr Opin Allergy Clin Immunol. 2014;14: 1–7.

7. García-Posadas L, Contreras-Ruiz L, Soriano-Romaní L, Dartt DA, Diebold Y. Conjunctival Goblet Cell Function: Effect of Contact Lens Wear and Cytokines. Eye Contact Lens. 2015. doi: 10.1097/ICL.0000000000000158 26067396

8. Knop E, Knop N. The role of eye-associated lymphoid tissue in corneal immune protection. J Anat. 2005. doi: 10.1111/j.1469-7580.2005.00394.x 15733300

9. Knop N, Knop E. Conjunctiva-associated lymphoid tissue in the human eye. Investig Ophthalmol Vis Sci. 2000 May;41(6):1270–9.

10. Agnifili L, Mastropasqua R, Fasanella V, Di Staso S, Mastropasqua A, Brescia L, et al. In vivo confocal microscopy of conjunctiva-associated lymphoid tissue in healthy humans. Investig Ophthalmol Vis Sci. 2014. doi: 10.1167/iovs.14-14365 25074770

11. Kahn CR, Young E, Lee Ihn Hwan, Rhim JS. Human corneal epithelial primary cultures and cell lines with extended life span: In vitro model for ocular studies. Investig Ophthalmol Vis Sci. 1993 Nov;34(12):3429–41.

12. Araki-Sasaki K, Ohashi Y, Sasabe T, Hayashi K, Watanabe H, Tano Y, et al. An SV40-immortalized human corneal epithelial cell line and its characterization. Investig Ophthalmol Vis Sci. 1995 Mar;36(3):614–21.

13. Gipson IK, Spurr-Michaud S, Argüeso P, Tisdale A, Ng TF, Russo CL. Mucin gene expression in immortalized human corneal-limbal and conjunctival epithelial cell lines. Investig Ophthalmol Vis Sci. 2003. doi: 10.1167/iovs.02-0851 12766048

14. Robertson DM, Li L, Fisher S, Pearce VP, Shay JW, Wright WE, et al. Characterization of growth and differentiation in a telomerase-immortalized human corneal epithelial cell line. Investig Ophthalmol Vis Sci. 2005. doi: 10.1167/iovs.04-0528 15671271

15. Diebold Y, Calonge M, De Salamanca AE, Callejo S, Corrales RM, Sáez V, et al. Characterization of a spontaneously immortalized cell line (IOBA-NHC) from normal human conjunctiva. Investig Ophthalmol Vis Sci. 2003. doi: 10.1167/iovs.03-0560 14507870

16. Capes-Davis A, Theodosopoulos G, Atkin I, Drexler HG, Kohara A, MacLeod RAF, et al. Check your cultures! A list of cross-contaminated or misidentified cell lines. Int J Cancer. 2010. doi: 10.1002/ijc.25242 20143388

17. Horbach SPJM, Halffman W. The ghosts of HeLa: How cell line misidentification contaminates the scientific literature. PLoS One. 2017. doi: 10.1371/journal.pone.0186281 29023500

18. Patterson JK, Lei XG, Miller DD. The Pig as an Experimental Model for Elucidating the Mechanisms Governing Dietary Influence on Mineral Absorption. Exp Biol Med. 2008. doi: 10.3181/0709-MR-262 18408137

19. Swindle MM, Makin A, Herron AJ, Clubb FJ, Frazier KS. Swine as Models in Biomedical Research and Toxicology Testing. Vet Pathol. 2012. doi: 10.1177/0300985811402846 21441112

20. Sanchez I, Martin R, Ussa F, Fernandez-Bueno I. The parameters of the porcine eyeball. Graefes Arch Clin Exp Ophthalmol. 2011. pp. 475–482. doi: 10.1007/s00417-011-1617-9 21287191

21. Lorget F, Parenteau A, Carrier M, Lambert D, Gueorguieva A, Schuetz C, et al. Characterization of the pH and temperature in the rabbit, pig, and monkey eye: Key parameters for the development of long-acting delivery ocular strategies. Mol Pharm. 2016;13: 2891–2896. doi: 10.1021/acs.molpharmaceut.5b00731 26655747

22. Hendrickson A, Hicks D. Distribution and density of medium- and short-wavelength selective cones in the domestic pig retina. Exp Eye Res. 2002. doi: 10.1006/exer.2002.1181 12076087

23. Funke S, Markowitsch S, Schmelter C, Perumal N, Mwiiri FK, Gabel-Scheurich S, et al. In-Depth Proteomic Analysis of the Porcine Retina by Use of a four Step Differential Extraction Bottom up LC MS Platform. Mol Neurobiol. 2017. doi: 10.1007/s12035-016-0172-0 27796761

24. Menduni F, Davies LN, Madrid-Costa D, Fratini A, Wolffsohn JS. Characterisation of the porcine eyeball as an in-vitro model for dry eye. Cont Lens Anterior Eye. 2018;41: 13–17. doi: 10.1016/j.clae.2017.09.003 28986008

25. Notara M, Schrader S, Daniels JT. The Porcine Limbal Epithelial Stem Cell Niche as a New Model for the Study of Transplanted Tissue-Engineered Human Limbal Epithelial Cells. Tissue Eng Part A. 2010. doi: 10.1089/ten.tea.2010.0343 20929285

26. Henker R, Scholz M, Gaffling S, Asano N, Hampel U, Garreis F, et al. Morphological Features of the Porcine Lacrimal Gland and Its Compatibility for Human Lacrimal Gland Xenografting. PLoS One. 2013;8. doi: 10.1371/journal.pone.0074046 24069265

27. Davanger M., Evensen A. Role of the Pericorneal Papillary Structure in Renewal of Corneal Epithelium. Nature 1971; 229: 560–561 doi: 10.1038/229560a0 4925352

28. Bron AJ, Tiffany JM. The meibomian glands and tear film lipids: structure, function and control. Adv Exp Med Biol 1998; 438:281–95. doi: 10.1007/978-1-4615-5359-5_40 9634898

29. Doughty MJ, Zaman ML. Human corneal thickness and its impact on intraocular pressure measures: a review and meta-analysis approach. Surv Ophthalmol. 2000;44:367–408. doi: 10.1016/s0039-6257(00)00110-7 10734239

30. Merindano MD, Costa J, Canals M, Potau JM, Ruano D. A comparative study of Bowman’s layer in some mammals: Relationships with other constituent corneal structures. Eur J Anat. 2002; 6 (3): 133–139.

31. Nautscher N, Bauer A, Steffl M, Amselgruber WM. Comparative morphological evaluation of domestic animal cornea. Vet Ophthalmol. 2016. doi: 10.1111/vop.12298 26190143

32. Gipson IK. Goblet cells of the conjunctiva: A review of recent findings. Prog Retin Eye Res. 2016. doi: 10.1016/j.preteyeres.2016.04.005 27091323

33. Kawano K, Uehara F, Ohba N. Lectin-cytochemical study on epithelial mucus glycoprotein of conjunctiva and pterygium. Exp Eye Res. 1988. doi: 10.1016/0014-4835(88)90022-X

34. Kessing S. Mucous gland system of the conjunctiva: a quantitative normal anatomical study. Acta Ophthalmol. Suppl. 1968,95: 1–133

35. Seftalıoglu A, Tezel G, Tezel T, Alabay B. Ultrastructural demonstration of helix pomatia lectin binding sites in goblet cells of human conjunctiva. Med J Islam World Acad Sci. 1993;6: 46–51.

36. Chodosh J, Nordquist RE, Kennedy RC. Comparative anatomy of mammalian conjunctival lymphoid tissue: A putative mucosal immune site. Dev Comp Immunol. 1998. doi: 10.1016/S0145-305X(98)00022-6

37. Wotherspoon A. C., Isaacson P. G., Hardman-Lea S. Mucosa-associated lymphoid tissue (MALT) in the human conjunctiva. J Pathol, 1994;174(1), 33–37. doi: 10.1002/path.1711740106 7965401

38. Dartt DA. The Conjunctiva—Structure and Function. Volume 2. Duane’s Foundations of Clinical Ophthalmology. Pennsylvania: Lipincott Williams and Wilkins; 2006.

39. Arends G, Schramm U. The structure of the human semilunar plica at different stages of its development—A morphological and morphometric study. Ann Anat. 2004. doi: 10.1016/S0940-9602(04)80002-5

40. Piehl M, Gilotti A, Donovan A, DeGeorge G, Cerven D. Novel cultured porcine corneal irritancy assay with reversibility endpoint. Toxicol Vitr. 2010. doi: 10.1016/j.tiv.2009.08.033 19735723

41. Alvarez-Trabado J, López-García A, Martín-Pastor M, Diebold Y, Sanchez A. Sorbitan ester nanoparticles (SENS) as a novel topical ocular drug delivery system: Design, optimization, and in vitro/ex vivo evaluation. Int J Pharm. 2018. doi: 10.1016/j.ijpharm.2018.05.015 29753904

42. Soriano-Romaní L, Álvarez-Trabado J, López-García A, Molina-Martínez I, Herrero-Vanrell R, Diebold Y. Improved in vitro corneal delivery of a thrombospondin-1-derived peptide using a liposomal formulation. Exp Eye Res. 2018. doi: 10.1016/j.exer.2017.12.002 29246497


Článek vyšel v časopise

PLOS One


2020 Číslo 1
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#