Histologic Features of Postnatal Development of Immune System Organs in the Sprague-Dawley Rat

Toxicologic Pathology

Volumn 43, Issue 6, 2015, Pages 794-815

  Parker, George A ^a   Picut, Catherine A ^a   Swanson, Cynthia ^a   Toot, Jonathan D ^b  

^a WIL Research   (United States)

^b WIL RESEARCH LABORATORIES   (United States)

Author keywords

histology; immune system; juvenile rats; perinatal development; postnatal development; Sprague Dawley rats

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AXILLARY LYMPH NODE; B LYMPHOCYTE; BIOLOGICAL PEST CONTROL; BONE MARROW; CELL DIFFERENTIATION; CELL POPULATION; ERYTHROPOIESIS; EXTRAMEDULLARY HEMATOPOIESIS; FEMALE; GERMINAL CENTER; HEMATOPOIETIC CELL; HISTOLOGY; IMMUNE SYSTEM; IMMUNOCOMPETENCE; INTESTINE LYMPHATIC TISSUE; JUVENILE ANIMAL; LYMPHOCYTE SUBPOPULATION; LYMPHOPOIESIS; MALE; MATURATION; MESENTERY LYMPH NODE; MONONUCLEAR CELL; MYELOPOIESIS; NASOPHARYNX; NONHUMAN; ORGANOGENESIS; PERINATAL PERIOD; PEYER PATCH; POPULATION DENSITY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SMALL INTESTINE; SPLEEN; SUBMANDIBULAR LYMPH NODE; T LYMPHOCYTE; THYMUS; YOUNG ADULT; AGING; ANIMAL; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LYMPH NODE; LYMPHOID TISSUE; NEWBORN; SPRAGUE DAWLEY RAT;

RATTUS;

AGING; ANIMALS; ANIMALS, NEWBORN; B-LYMPHOCYTES; BONE MARROW; FEMALE; IMMUNE SYSTEM; LYMPH NODES; LYMPHOID TISSUE; MALE; RATS; RATS, SPRAGUE-DAWLEY; SPLEEN; T-LYMPHOCYTES; THYMUS GLAND;

EID: 84938596350     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623315578720     Document Type: Article

References (91)

1. Abo T. (2001). Extrathymic pathways of T-cell differentiation and immunomodulation. Int Immunopharmacol 1, 1261–73.
2. Aboussaouira T. Moustafa Y. Idelman S. (1988). Image analysis of cell proliferation in rat thymus throughout development. Thymus 12, 167–86.
3. Adachi S. Yoshida H. Kataoka H. Nishikawa S. (1997). Three distinctive steps in Peyer’s patch formation of murine embryo. Int Immunol 9, 507–14.
4. Arno J. (1980). Atlas of Lymph Node Pathology. Lippincott, Philadelphia, PA.
5. Beagley K. W. Elson C. O. (1992). Cells and cytokines in mucosal immunity and inflammation. Gastroenterol Clin North Am 21, 347–66.
6. Belkaid Y. (2013). The mucosal immune system. In Fundamental Immunology (Paul W. E., ed.), pp. 833–49. Wolters Kluwer/Lippincott Williams & Wilkins, Philadelphia, PA.
7. Bruder M. C. Spanhaak S. Bruijntjes J. P. Michielsen C. P. Vos J. G. Kuper C. F. (1999). Intestinal T lymphocytes of different rat strains in immunotoxicity. Toxicol Pathol 27, 171–79.
8. Bunn T. L. Ladics G. S. Holsapple M. P. Dietert R. R. (2001). Developmental immunotoxicity assessment in the rat: Age, gender, and strain comparisons after exposure to lead. Toxicol Methods 11, 41–58.
9. Bunn T. L. Parsons P. J. Kao E. Dietert R. R. (2001a). Exposure to lead during critical windows of embryonic development: Differential immunotoxic outcome based on stage of exposure and gender. Toxicol Sci 64, 57–66.
10. Bunn T. L. Parsons P. J. Kao E. Dietert R. R. (2001b). Gender-based profiles of developmental immunotoxicity to lead in the rat: Assessment in juveniles and adults. J Toxicol Environ Health A 64, 223–40.
11. Burns-Naas L. A. Hastings K. L. Ladics G. S. Makris S. L. Parker G. A. Holsapple M. P. (2008). What’s so special about the developing immune system? Int J Toxicol 27, 223–54.
12. Cesta M. F. (2006a). Normal structure, function, and histology of mucosa-associated lymphoid tissue. Toxicol Pathol 34, 599–608.
13. Cesta M. F. (2006b). Normal structure, function, and histology of the spleen. Toxicol Pathol 34, 455–65.
14. Chang T. K. Bellward G. D. (1996). Peripubertal androgen imprinting of rat hepatic cytochrome P450 2C11 and steroid 5 alpha-reductase: Pretranslational regulation and impact on microsomal drug activation. J Pharmacol Exp Ther 278, 1383–91.
15. Chen D. Hoshi H. Tanaka K. Murakami G. (1995). Postnatal development of lymphoid follicles in rat Peyer’s patches, with special reference to increased follicle number. Arch Histol Cytol 58, 335–43.
16. Cheroutre H. (2005). IELs: Enforcing law and order in the court of the intestinal epithelium. Immunol Rev 206, 114–31.
17. Crouse D. A. Perry G. A. Murphy B. O. Sharp J. G. (1989). Characteristics of submucosal lymphoid tissue located in the proximal colon of the rat. J Anat 162, 53–65.
18. Csencsits K. L. Jutila M. A. Pascual D. W. (1999). Nasal-associated lymphoid tissue: Phenotypic and functional evidence for the primary role of peripheral node addressin in naive lymphocyte adhesion to high endothelial venules in a mucosal site. J Immunol 163, 1382–89.
19. Cumano A. Ferraz J. C. Klaine M. Di Santo J. P. Godin I. (2001). Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity 15, 477–85.
20. Cumano A. Godin I. (2001). Pluripotent hematopoietic stem cell development during embryogenesis. Curr Opin Immunol 13, 166–71.
21. Diaz-Jouanen E. Williams R. C. Jr. (1974). T and B lymphocytes in human colostrum. Clin Immunol Immunopath 3, 248–55.
22. Elmore S. A. (2006a). Enhanced histopathology of mucosa-associated lymphoid tissue. Toxicol Pathol 34, 687–96.
23. Elmore S. A. (2006b). Enhanced histopathology of the bone marrow. Toxicol Pathol 34, 666–86.
24. Elmore S. A. (2006c). Enhanced histopathology of the lymph nodes. Toxicol Pathol 34, 634–47.
25. Elmore S. A. (2006d). Enhanced histopathology of the spleen. Toxicol Pathol 34, 648–55.
26. Elmore S. A. (2006e). Enhanced histopathology of the thymus. Toxicol Pathol 34, 656–65.
27. Elmore S. A. (2006f). Histopathology of the lymph nodes. Toxicol Pathol 34, 425–54.
28. Elmore S. A. (2012). Enhanced histopathology of the immune system: A review and update. Toxicol Pathol 40, 148–56.
29. Endt K. Stecher B. Chaffron S. Slack E. Tchitchek N. Benecke A. Van Maele L. (2010). The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLoS Pathog 6, e1001097.
30. Fukuyama S. Hiroi T. Yokota Y. Rennert P. D. Yanagita M. Kinoshita N. Terawaki S. (2002). Initiation of NALT organogenesis is independent of the IL-7R, LTbetaR, and NIK signaling pathways but requires the Id2 gene and CD3(−)CD4(+)CD45(+) cells. Immunity 17, 31–40.
31. Gehrs B. C. Smialowicz R. J. (1999). Persistent suppression of delayed-type hypersensitivity in adult F344 rats after perinatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicology 134, 79–88.
32. Godin I. Garcia-Porrero J. A. Dieterlen-Lievre F. Cumano A. (1999). Stem cell emergence and hemopoietic activity are incompatible in mouse intraembryonic sites. J Exp Med 190, 43–52.
33. Hamada H. Hiroi T. Nishiyama Y. Takahashi H. Masunaga Y. Hachimura S. Kaminogawa S. (2002). Identification of multiple isolated lymphoid follicles on the antimesenteric wall of the mouse small intestine. J Immunol 168, 57–64.
34. Hameleers D. M. van der Ende M. Biewenga J. Sminia T. (1989). An immunohistochemical study on the postnatal development of rat nasal-associated lymphoid tissue (NALT). Cell Tissue Res 256, 431–38.
35. Harland J. (1940). Early histogenesis of the thymus in the white rat. Anat Rec 77, 247–71.
36. Hashi H. Yoshida H. Honda K. Fraser S. Kubo H. Awane M. Takabayashi A. Nakano H. Yamaoka Y. Nishikawa S. (2001). Compartmentalization of Peyer’s patch anlagen before lymphocyte entry. J Immunol 166, 3702–9.
37. Hayday A. Theodoridis E. Ramsburg E. Shires J. (2001). Intraepithelial lymphocytes: Exploring the hird Way in immunology. Nat Immunol 2, 997–1003.
38. Holsapple M. P. (2002). Developmental immunotoxicology and risk assessment: A workshop summary. Human Exp Toxicol 21, 473–78.
39. Holsapple M. P. (2003). Developmental immunotoxicity testing: A review. Toxicology 185, 193–203.
40. Holsapple M. P. West L. J. Landreth K. S. (2003). Species comparison of anatomical and functional immune system development. Birth Defects Res Part B Dev Reprod Toxicol 68, 321–34.
41. Hooper L. V. Macpherson A. J. (2010). Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 10, 159–69.
42. Institute for Laboratory Animal Research. (2010). Guide for the Care and Use of Laboratory Animals, Eighth Edition. The National Academies Press, Washington, DC.
43. Jung C. Hugot J. P. Barreau F. (2010). Peyer’s patches: The immune sensors of the intestine. Int J Inflam 2010, 823710.
44. M.H., Kaufman, J.J.L., Bard, The Anatomical Basis of Mouse Development, Elsevier-Academic Press, San Diego, CA, (1999)
45. Kikkawa Y. Fujita I. Sindhu R. K. (1994). Neonatal hyperoxia and cytochrome P450 imprinting in adulthood. Pediatr Res 35, 255–58.
46. Kincade P. W. (1981). Formation of B lymphocytes in fetal and adult life. Adv Immunol 31, 177–245.
47. Kiyono H. Fukuyama S. (2004). NALT- versus Peyer’s-patch-mediated mucosal immunity. Nat Rev Immunol 4, 699–710.
48. Kodama R. Okazaki T. Sato T. Iwashige S. Tanigawa Y. Fujishima J. Moriyama A. (2012). Age difference in morphology and immunohistology in the Thymus and Spleen in Crl:CD (SD) rats. J Toxicol Pathol 25, 55–61.
49. Kuper C. F. Hameleers D. M. Bruijntjes J. P. van der Ven I. Biewenga J. Sminia T. (1990). Lymphoid and non-lymphoid cells in nasal-associated lymphoid tissue (NALT) in the rat. An immuno- and enzyme-histochemical study. Cell Tissue Res 259, 371–77.
50. Kuper C. F. Koornstra P. J. Hameleers D. M. Biewenga J. Spit B. J. Duijvestijn A. M. van Breda Vriesman P. J. Sminia T. (1992). The role of nasopharyngeal lymphoid tissue. Immunology Today 13, 219–24.
51. Kuper C. F. Ruehl-Fehlert C. Elmore S. A. Parker G. A. (2013). Immune system. In Haschek and Rousseaux’s Handbook of Toxicologic Pathology (Haschek W. M. Rousseaux C. G. Wallig M. A., eds.), Vol. 2, pp. 1795–862. Elsevier London.
52. Kuper C. F. Van Zijverden M. Klaassen C. Tegelenbosch-Schouten M. Wolterbeek A. P. (2007). Effects of cyclosporin A and cyclophosphamide on Peyer’s patches in rat, exposed in utero and neonatally or during adult age. Toxicol Pathol 35, 226–32.
53. Ladics G. S. Smith C. Bunn T. L. Dietert R. R. Anderson P. K. Wiescinski C. M. Holsapple M. P. (2000). Characterization of an approach to developmental immunotoxicology assessment in the rat using SRBC as the antigen. Toxicol Methods 10, 283–311.
54. Landreth K. S. (1993). B lymphocyte development as a developmental process. In Developmental Immunology (Cooper E. L. Brown E. N., eds.), pp. 238–73. Oxford University Press, New York.
55. Landreth K. S. (2002). Critical windows in development of the rodent immune system. Hum Exp Toxicol 21, 493–98.
56. Lehner T. Panagiotidi C. Bergmeier L. A. Tao L. Brookes R. Gearing A. Adams S. (1995). Genital-associated lymphoid tissue in female non-human primates. Adv Exp Med Biol 371A, 357–65.
57. Losco P. Harlemen H. (1992). Normal development, growth and aging of the lymph node. In Pathobiology of the Aging Rat (Mohr U. Dungworth D. L. Capen C. C., eds.), Vol. 1, pp. 49–73. ILSI Press, Washington, DC.
58. Lugering A. Kucharzik T. (2006). Induction of intestinal lymphoid tissue: The role of cryptopatches. Ann NY Acad Sci 1072, 210–17.
59. Lyscom N. Brueton M. J. (1983). The development of intraepithelial and Peyer’s patch lymphocyte sub-types in the small intestine of newborn rats. Clin Exp Immunol 54, 158–62.
60. Miller T. E. Golemboski K. A. Ha R. S. Bunn T. Sanders F. S. Dietert R. R. (1998). Developmental exposure to lead causes persistent immunotoxicity in Fischer 344 rats. Toxicol Sci 42, 129–35.
61. Moghaddami M. Cummins A. Mayrhofer G. (1998). Lymphocyte-filled villi: Comparison with other lymphoid aggregations in the mucosa of the human small intestine. Gastroenterology 115, 1414–25.
62. Moolenbeek C. Ruitenberg E. J. (1981). The “Swiss roll”: A simple technique for histological studies of the rodent intestine. Lab Anim 15, 57–59.
63. Mustafa A. Holladay S. D. Witonsky S. Zimmerman K. Reilly C. M. Sponenberg D. P. Weinstein D. A. Karpuzoglu E. Gogal R. M. Jr. (2009). Gestational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin disrupts B-cell lymphopoiesis and exacerbates autoimmune disease in 24-week-old SNF1 mice. Toxicol Sci 112, 133–43.
64. O’Hara A. M. Shanahan F. (2006). The gut flora as a forgotten organ. EMBO Rep 7, 688–93.
65. Pabst O. Herbrand H. Worbs T. Friedrichsen M. Yan S. Hoffmann M. W. Korner H. Bernhardt G. Pabst R. Forster R. (2005). Cryptopatches and isolated lymphoid follicles: Dynamic lymphoid tissues dispensable for the generation of intraepithelial lymphocytes. Eur J Immunol 35, 98–107.
66. Paige C. J. Kincade P. W. Shinefeld L. A. Sato V. L. (1981). Precursors of murine B lymphocytes. Physical and functional characterization, and distinctions from myeloid stem cells. J Exp Med 153, 154–65.
67. Parker G. A. Picut C. A. (2005). Liver immunobiology. Toxicol Pathol 33, 52–62.
68. Parker G. A. Picut C. A. (2012). Immune functioning in non lymphoid organs: The liver. Toxicol Pathol 40, 237–47.
69. Pearse G. (2006a). Histopathology of the thymus. Toxicol Pathol 34, 515–47.
70. Pearse G. (2006b). Normal structure, function and histology of the thymus. Toxicol Pathol 34, 504–14.
71. Porgador A. Staats H. F. Itoh Y. Kelsall B. L. (1998). Intranasal immunization with cytotoxic T-lymphocyte epitope peptide and mucosal adjuvant cholera toxin: Selective augmentation of peptide-presenting dendritic cells in nasal mucosa-associated lymphoid tissue. Infect Immun 66, 5876–81.
72. Randall T. D. (2010). Bronchus-associated Lymphoid Tissue (BALT) structure and function. Adv Immunol 107, 187–241.
73. Rangel-Moreno J. Carragher D. M. de la Luz Garcia-Hernandez M. Hwang J. Y. Kusser K. Hartson L. Kolls J. K. Khader S. A. Randall T. D. (2011). The development of inducible bronchus-associated lymphoid tissue depends on IL-17. Nat Immunol 12, 639–46.
74. Reynolds J. D. Morris B. (1983). The evolution and involution of Peyer’s patches in fetal and postnatal sheep. Eur J Immunol 13, 627–35.
75. Richie E. R. Bass R. Meistrich M. L. Dennison D. K. (1982). Distribution of T lymphocyte subsets in human colostrum. J Immunol 129, 1116–19.
76. Savilahti E. (1972). Immunoglobulin-containing cells in the intestinal mucosa and immunoglobulins in the intestinal juice in children. Clin Exp Immunol 11, 415–25.
77. Seelig L. L. Jr Billingham R. E. (1981). Capacity of “transplanted” lymphocytes to traverse the intestinal epithelium of adult rats. Transplantation 32, 308–14.
78. Singh A. Yadav S. Srivastava V. Kumar R. Singh D. Sethumadhavan R. Parmar D. (2013). Imprinting of cerebral and hepatic cytochrome p450s in rat offsprings exposed prenatally to low doses of cypermethrin. Mol Neurobiol 48, 128–40.
79. Sminia T. Janse E. M. Plesch B. E. (1983). Ontogeny of Peyer’s patches of the rat. Anat Rec 207, 309–16.
80. Spit B. J. Hendriksen E. G. Bruijntjes J. P. Kuper C. F. (1989). Nasal lymphoid tissue in the rat. Cell Tissue Res 255, 193–98.
81. Suttie A. W. (2006). Histopathology of the spleen. Toxicol Pathol 34, 466–503.
82. Tizard I. (1987). An Introduction of Veterinary Immunology. Saunders, Philadelphia, PA.
83. Travlos G. S. (2006). Normal structure, function, and histology of the bone marrow. Toxicol Pathol 34, 548–65.
84. Van Kruiningen H. J. West A. B. Freda B. J. Holmes K. A. (2002). Distribution of Peyer’s patches in the distal ileum. Inflamm Bowel Dis 8, 180–85.
85. van Rees E. P. Dijkstra C. D. van Rooijen N. (1986). The early postnatal development of the primary immune response in TNP-KLH-stimulated popliteal lymph node in the rat. Cell Tissue Res 246, 673–77.
86. van Rees E. P. Dijkstra C. D. van Rooijen N. (1987). The early postnatal development of the primary immune response in rat popliteal lymph node, stimulated with thymus-independent type-1 and type-2 antigens. Cell Tissue Res 250, 695–99.
87. van Rees E. P. Dopp E. A. Dijkstra C. D. Sminia T. (1985). The postnatal development of cell populations in the rat popliteal lymph node. An immunohistochemical study. Cell Tissue Res 242, 391–98.
88. Weinstein D. A. Gogal R. M. Jr Mustafa A. Prater M. R. Holladay S. D. (2008). Mid-gestation exposure of C57BL/6 mice to 2,3,7,8-tetrachlorodibenzo-p-dioxin causes postnatal morphologic changes in the spleen and liver. Toxicol Pathol 36, 705–13.
89. Weinstock D. Lewis D. B. Parker G. A. Beyer J. Collinge M. Brown T. P. Dybdal N. (2010). Toxicopathology of the developing immune system: Investigative and development strategies. Toxicol Pathol 38, 1111–17.
90. Willard-Mack C. L. (2006). Normal structure, function, and histology of lymph nodes. Toxicol Pathol 34, 409–24.
91. Yuki Y. Kiyono H. (2003). New generation of mucosal adjuvants for the induction of protective immunity. Rev Med Virol 13, 293–310.