Ultrastructural anatomy of CALT follicles in the rabbit reveal characteristics of M-cells, germinal centres and high endothelial venules

Journal of Anatomy

Volumn 207, Issue 4, 2005, Pages 409-426

  Knop, Nadja ^a   Knop, Erich ^b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Conjunctiva associated lymphoid tissue (CALT); Eye associated lymphoid tissue (EALT); High endothelial venules (HEV); Lymphoid follicles; M cells; Mucosal immunity

Indexed keywords

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ULTRASTRUCTURE; CONJUNCTIVA; CONTROLLED STUDY; CYTOPLASM; EPITHELIUM CELL; FOLLICULAR DENDRITIC CELL; GERMINAL CENTER; GOBLET CELL; LOWER EYELID; LYMPH FOLLICLE; LYMPHOBLAST; LYMPHOCYTE MIGRATION; LYMPHOID TISSUE; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; RABBIT; SCANNING ELECTRON MICROSCOPY; STAINING; TISSUE STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; VENULE;

ANIMALS; APOPTOSIS; CONJUNCTIVA; DENDRITIC CELLS, FOLLICULAR; ENDOTHELIAL CELLS; EPITHELIAL CELLS; GERMINAL CENTER; IMMUNITY, MUCOSAL; LYMPHATIC VESSELS; LYMPHOCYTES; LYMPHOID TISSUE; MACROPHAGES; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; RABBITS; TISSUE FIXATION;

ORYCTOLAGUS CUNICULUS;

EID: 26944481070     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2005.00470.x     Document Type: Article

References (76)

1. Anderson AO, Anderson ND (1976) Lymphocyte emigration from high endothelial venules in rat lymph nodes. Immunology 31, 731-748.
2. Astley RA, Chodosh J (2005) Selective uptake of iron oxide by rabbit conjunctival lymphoid follicles. Cornea 24, 334-336.
3. Aurell G (1938) Kolophonium-Chininhydrochloridgemische als Einschlussmittel für sehr dicke Schnitte zu mikroskopischen Zwecken. Z. Wiss Mikr 55, 256-273.
4. Axelrod AJ, Chandler JW (1979) Morphologic characteristics of conjunctival lymphoid tissue in the rabbit. In Proceedings of the Second International Symposium on the Immunology and Immunopathology of the Eye (eds Silverstein AM, Connor GR), pp. 292-301. New York: Masson Publishing.
5. Bielory L, Mongia A (2002) Current opinion of immunotherapy for ocular allergy. Curr Opin Allergy Clin Immunol 2, 447-452.
6. Bienenstock J, McDermott M, Befus D, O'Neill M (1978) A common mucosal immunologic system involving the bronchus, breast and bowel. Adv Exp Med Biol 107, 53-59.
7. Brandtzaeg P (1996) History of oral tolerance and mucosal immunity. Ann NY Acad Sci 778, 1-27.
8. Butcher EC, Picker LJ (1996) Lymphocyte homing and homeostasis. Science 272, 60-66.
9. Bye WA, Allan CH, Trier JS (1984) Structure, distribution, and origin of M cells in Peyer's patches of mouse ileum. Gastroenterology 86, 789-801.
10. Chandler JW, Axelrod AJ (1980) Conjunctiva-associated lymphoid tissue: a probable component of the mucosa-associated lymphoid system. In Immunologic Diseases of the Mucous Membrane: Pathology, Diagnosis and Treatment (ed. Connor GR), pp. 63-70. New York: Masson Publishing.
11. Chodosh J, Nordquist RE, Kennedy RC (1998a) Anatomy of mammalian conjunctival lymphoepithelium. Adv Exp Med Biol 438, 557-565.
12. Chodosh J, Nordquist RE, Kennedy RC (1998b) Comparative anatomy of mammalian conjunctival lymphoid tissue: a putative mucosal immune site. Dev Comp Immunol 22, 621-630.
13. Chodosh J, Kennedy RC (2002) The conjunctival lymphoid follicle in mucosal immunology. DNA Cell Biol 21, 421-433.
14. Dana MR, Qian Y, Hamrah P (2000) Twenty-five-year panorama of corneal immunology: emerging concepts in the immunopathogenesis of microbial keratitis, peripheral ulcerative keratitis, and corneal transplant rejection. Cornea 19, 625-643.
15. Debard N, Sierro F, Kraehenbuhl JP (1999) Development of Peyer's patches, follicle-associated epithelium and M cell: lessons from immunodeficient and knockout mice. Semin Immunol 11, 183-191.
16. Dua HS, Donoso LA, Laibson PR (1994) Conjunctival instillation of retinal antigens induces tolerance. Ocular Immunol Inflammation 2, 29-36.
17. Farstad IN, Halstensen TS, Fausa O, Brandtzaeg P (1994) Heterogeneity of M-cell-associated B and T cells in human Peyer's patches. Immunology 83, 457-464.
18. Franklin RM, Remus LE (1984) Conjunctival-associated lymphoid tissue: evidence for a role in the secretory immune system. Invest Ophthalmol Vis Sci 25, 181-187.
19. Gebert A, Bartels H (1990) Ultrastruktur des follikel-assoziierten Epithels in der Konjunktiva des Kaninchens. Verh Anat Ges (Anat Anz Suppl) 166, 359-360.
20. Gebert A, Hach G (1992) Vimentin antibodies stain membranous epithelial cells in the rabbit bronchus-associated lymphoid tissue (BALT). Histochemistry 98, 271-273.
21. Gebert A, Bartels H (1995) Ultrastructure and protein transport of M cells in the rabbit cecal patch. Anat Rec 241, 487-495.
22. Gebert A, Willfuhr B, Pabst R (1995) The rabbit M-cell marker vimentin is present in epithelial cells of the tonsil crypt. Acta Otolaryngol Stockh 115, 697-700.
23. Gebert A, Rothkotter HJ, Pabst R (1996) M cells in Peyer's patches of the intestine. Int Rev Cytol 167, 91-159.
24. Gebert A (1997) The role of M cells in the protection of mucosal membranes. Histochem Cell Biol 108, 455-470.
25. Gebert A, Posselt W (1997) Glycoconjugate expression defines the origin and differentiation pathway of intestinal M-cells. J Histochem Cytochem 45, 1341-1350.
26. Giuliano EA, Moore CP, Phillips TE (2002) Morphological evidence of M cells in healthy canine conjunctiva-associated lymphoid tissue. Graefes Arch Clin Exp Ophthalmol 240, 220-226.
27. Gowans JL, Knight EJ (1964) The route of re-circulation of lymphocytes in the rat. Proc Soc Exp Biol Med 159, 257-282.
28. Gullberg E, Leonard M, Karlsson J, et al. (2000) Expression of specific markers and particle transport in a new human intestinal M-cell model. Biochem Biophys Res Commun 279, 808-813.
29. Hamzaoui N, Pringault E (1998) Interaction of microorganisms, epithelium, and lymphoid cells of the mucosa-associated lymphoid tissue. Ann NY Acad Sci 859, 65-74.
30. Haynes RJ, Tighe PJ, Scott RA, Dua HS (1999) Human conjunctiva contains high endothelial venules that express lymphocyte homing receptors. Exp Eye Res 69, 397-403.
31. Howie AJ (1980) Scanning and transmission electron microscopy on the epithelium of human palatine tonsils. J Pathol 130, 91-98.
32. Jepson MA, Clark MA, Simmons NL, Hirst BH (1993) Epithelial M cells in the rabbit caecal lymphoid patch display distinctive surface characteristics. Histochemistry 100, 441-447.
33. Jepson MA, Clark MA, Hirst BH (2004) M cell targeting by lectins: a strategy for mucosal vaccination and drug delivery. Advanced Drug Delivery Rev 56, 511-525.
34. Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27, 137-138.
35. Kessing SV (1968) Mucous gland system of the conjunctiva. A quantitative normal anatomical study. Acta Ophthalmol Copenh Suppl 95, 1-133.
36. Knop E, Knop N (1996) MALT tissue of the conjunctiva and nasolacrimal system in the rabbit and human. Vision Res 36, S60.
37. Knop E, Knop N (1998a) Fine structure of high endothelial venules in the human conjunctiva. Ophthalmic Res 30, 169.
38. Knop E, Knop N (1998b) High endothelial venules are a normal component of lymphoid tissue in the human conjunctiva and lacrimal sac. Invest Ophthalmol Vis Sci 39, S548.
39. Knop N, Knop E (1998c) Cells with m-cell characteristics in the follicle associated epithelium of the rabbit conjunctiva. Ophthalmic Res 30 (Suppl. 1, 392), 82.
40. Knop N, Knop E (1998d) M-cells of the conjunctiva associated lymphoid tissue (CALT) in the rabbit and human. Invest Ophthalmol Vis Sci 39, 548.
41. Knop N, Knop E (2000) Conjunctiva-associated lymphoid tissue in the human eye. Invest Ophthalmol Vis Sci 41, 1270-1279.
42. Knop E, Knop N (2001) Lacrimal drainage associated lymphoid tissue (LDALT): A part of the human mucosal immune system. Invest Ophthalmol Vis Sci 42, 566-574.
43. Knop E, Knop N (2002) A functional unit for ocular surface immune defense formed by the lacrimal gland, conjunctiva and lacrimal drainage system. Adv Exp Med Biol 506, 835-844.
44. Knop E, Knop N (2003) Augen-assoziiertes lymphatisches Gewebe (EALT) durchzieht die Augenoberfläche kontinuierlich von der Tränendrüse bis in die ableitenden Tränenwege. Ophthalmologe 100, 929-942.
45. Knop E, Knop N, Brewitt H (2003) [Dry eye disease as a complex dysregulation of the functional anatomy of the ocular surface. New impulses to understanding dry eye disease]. Ophthalmologe 100, 917-928.
46. Knop E, Knop N (2004a) Eye associated lymphoid tissue (EALT) and the ocular surface. In Proceedings of the 5th International Symposium on Ocular Pharmacology and Therapy, pp. 91-98. Bologna: Medimond.
47. Knop E, Knop N (2004b) Lymphocyte homing in the mucosal immune system to the eye-associated lymphoid tissue (EALT). In Immunology of the Ocular Surface and Tearfilm (eds Zierhut M, Sullivan DA, Stern ME), pp. 35-72. Amsterdam: Swets and Zeitlinger.
48. Knop E, Knop N, Pleyer U (2004) Clinical aspects of MALT. In Uveitis and Immunological Disorders (eds Pleyer U, Mondino B), pp. 67-89. Berlin: Springer Verlag.
49. Knop E, Knop N (2005) The role of eye-associated lymphoid tissue in corneal immune protection. J Anat 206, 271-285.
50. Kraal G, Mebius RE (1997) High endothelial venules: lymphocyte traffic control and controlled traffic. Adv Immunol 65, 347-395.
51. Kraehenbuhl JP, Neutra MR (2000) Epithelial M cells: differentiation and function. Annu Rev Cell Dev Biol 16, 301-332.
52. Latkovic S (1989) Ultrastructure of M cells in the conjunctival epithelium of the guinea pig. Curr Eye Res 8, 751-755.
53. Liu H, Meagher CK, Moore CP, Phillips TE (2004) Antigen sampling M cells in the rabbit conjunctiva. Invest Ophthalmol Visual Sci 45, 1505.
54. van der Lubben I, van Opdorp FA, Hengeveld MR, et al. (2002) Transport of chitosan microparticles for mucosal vaccine delivery in a human intestinal M-cell model. J Drug Target 10, 449-456.
55. McGhee JR, Lamm ME, Strober W (1999) Mucosal immune responses. An overview. In Handbook of Mucosal Immunology (eds Ogra PL, Mestecky J, Lamm ME, Strober W, McGhee JR, Bienenstock J), pp. 485-506. San Diego: Academic Press.
56. Mestecky J, McGhee JR, Michalek SM, Arnold RR, Crago SS, Babb JL (1978) Concept of the local and common mucosal immune response. Adv Exp Med Biol 107, 185-192.
57. Neutra MR, Frey A, Kraehenbuhl JP (1996a) Epithelial M cells: gateways for mucosal infection and immunization. Cell 86, 345-348.
58. Neutra MR, Pringault E, Kraehenbuhl JP (1996b) Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol 14, 275-300.
59. Niimi Y (1935) Studien über den Lymphfollikel in der Conjunctiva. I. Mitt. Über den Lymphfollikel in der Conjunctiva bei normalen Kaninchen. Acta Soc Ophthal Japan 39, 808-823.
60. Nunez JA, Cuesta U (2000) Local conjunctival immunotherapy: the effect of dermatophagoides pteronyssinus local conjunctival immunotherapy on conjunctival provocation test in patients with allergic conjunctivitis. Allergol Immunopathol (Madr) 28, 301-306.
61. Olah I, Takacs L, Toro I (1988) Formation of lymphoepithelial tissue in the sheep's palatine tonsil. Acta Otolaryngol Suppl 454, 7-17.
62. Owen RL, Jones AL (1974) Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66, 189-203.
63. Pabst R, Westermann J (1997) Lymphocyte traffic to lymphoid and non-lymphoid organs in different species is regulated by several mechanisms. In Adhesion Molecules and Chemokines in Lymphocyte Trafficking (ed. Hamann, A), pp. 21-37. Amsterdam: Harwood Academic Publishers.
64. Paulsen FP, Paulsen JI, Thale AB, Schaudig U, Tillmann BN (2002) Organized mucosa-associated lymphoid tissue in human naso-lacrimal ducts. Adv Exp Med Biol 506, 873-876.
65. Pflugfelder SC, Solomon A, Stern ME (2000) The diagnosis and management of dry eye: a twenty-five-year review. Cornea 19, 644-649.
66. Ruskell GL (1995) Organization and cytology of lymphoid tissue in the cynomolgus monkey conjunctiva. Anat Rec 243, 153-164.
67. Ruskell GL, VanderWerf F (1997) Sensory innervation of conjunctival lymph follicles in cynomolgus monkeys. Invest Ophthalmol Vis Sci 38, 884-892.
68. Shoji J, Inada N, Saito K, Takaura N, Iwasaki Y, Sawa M (1998) Immunohistochemical study on follicular dendritic cell of conjunctiva-associated lymphoid tissue. Jpn J Ophthalmol 42, 1-7.
69. Smith ME, Finke EH (1972) Critical point drying of soft biological material for the scanning electron microscope. Invest Ophthalmol Visual Sci 11, 127-132.
70. Smith MW, Peacock MA (1992) Microvillus growth and M-cell formation in mouse Peyer's patch follicle-associated epithelial tissue. Exp Physiol 77, 389-392.
71. Stern ME, Gao J, Schwalb TA, et al. (2002) Conjunctival T-cell subpopulations in Sjogren's and non-Sjogren's patients with dry eye. Invest Ophthalmol Vis Sci 43, 2609-2614.
72. Stock EL, Sobut RA, Roth SI (1987) The uptake of horseradish peroxidase by the conjunctival epithelium of the guinea-pig. Exp Eye Res 45, 327-337.
73. Szakal AK, Holmes KL, Tew JG (1983) Transport of immune complexes from the subcapsular sinus to lymph node follicles on the surface of nonphagocytic cells, including cells with dendritic morphology. J Immunol 131, 1714-1727.
74. Virchow H (1910) Mikroskopische Anatomie der äusseren Augenhaut und des Lidapparates. In Graefe-Saemisch Handbuch der Gesamten Augenheilkunde, Band 1, 1 Abteilung, Kapitel II (ed. Saemisch T), p. 431. Leibzig: Verlag W. Engelmann.
75. Wolf JL, Rubin DH, Finberg R, et al. (1981) Intestinal M cells: a pathway for entry of reovirus into the host. Science 212, 471-472.
76. Wolniak KL, Shinall SM, Waldschmidt TJ (2004) The germinal center response. Crit Rev Immunol 24, 39-65.