TY - JOUR
T1 - Organogenesis of Ileal Peyer's Patches Is Initiated Prenatally and Accelerated Postnatally With Comprehensive Proliferation of B Cells in Pigs
AU - Furukawa, Mutsumi
AU - Ito, Shun
AU - Suzuki, Shunichi
AU - Fuchimoto, Daiichiro
AU - Onishi, Akira
AU - Niimi, Kanae
AU - Usami, Katsuki
AU - Wu, Guoyao
AU - Bazer, Fuller W.
AU - Ogasawara, Kouetsu
AU - Watanabe, Kouichi
AU - Aso, Hisashi
AU - Nochi, Tomonori
N1 - Funding Information:
We thank Mitsuji Kaji and Hiromi Yoshida (Tohoku University Institute of Development, Aging and Cancer), Makoto Osada and Kazue Nagasawa (Tohoku University Graduate School of Agricultural Science), and the staff (Keyence) for their technical support to obtain tissue images.
Funding Information:
This study was mostly supported by the Rare/Intractable Disease Project of Japan from The Japan Agency for Medical Research and Development (AMED). This study was also supported in part by the Grants-in-Aid for Scientific Research (A) (18H03969), for the Japan Society for the Promotion of Science (JSPS) fellow (19J11689), and the Core-to-Core Program (Advanced Research Networks) from JSPS, the Program for Interdisciplinary Research from Frontier Research Institute for Interdisciplinary Sciences at Tohoku University, and the Grant for Joint Research Project of Institute of Development, Aging and Cancer, Tohoku University.
Publisher Copyright:
© Copyright © 2020 Furukawa, Ito, Suzuki, Fuchimoto, Onishi, Niimi, Usami, Wu, Bazer, Ogasawara, Watanabe, Aso and Nochi.
PY - 2020/12/4
Y1 - 2020/12/4
N2 - Morphogenesis and differentiation of organs is required for subsequent functional maturation. The morphological features of Peyer's patches vary among species. In pigs, they develop extensively in the ileum as ileal Peyer's patches (IPPs). However, the role of IPPs in the porcine immune system remains to be elucidated because of a lack of complete understanding of IPP organogenesis. Results of the present study revealed that development of porcine IPPs is initiated prenatally between embryonic days 76 and 91. The process of IPP organogenesis is concomitant with increased transcriptional patterns of CXCL13 and CCL19. IPPs undergo further development postnatally by forming central, marginal, and subepithelial zones. Importantly, a large number of proliferating B cells and apoptotic cells are found in porcine IPPs postnatally, but not prenatally. The expression level of IgM in proliferating B cells depends on the zone in which distinct B cells are separately localized after birth. Specifically, IgM+ cells are predominantly found in the central zone, whereas IgM-/low cells are abundant in the marginal zone. Importantly, the cellular feature of IPPs differs from that of mesenteric lymph nodes (MLNs) where such distinct zones are not formed both prenatally and postnatally. Our findings suggest that IPPs (not MLNs) in postnatal pigs are involved in complementing functions of the primary lymphoid tissue that promotes the differentiation and maturation of B cells.
AB - Morphogenesis and differentiation of organs is required for subsequent functional maturation. The morphological features of Peyer's patches vary among species. In pigs, they develop extensively in the ileum as ileal Peyer's patches (IPPs). However, the role of IPPs in the porcine immune system remains to be elucidated because of a lack of complete understanding of IPP organogenesis. Results of the present study revealed that development of porcine IPPs is initiated prenatally between embryonic days 76 and 91. The process of IPP organogenesis is concomitant with increased transcriptional patterns of CXCL13 and CCL19. IPPs undergo further development postnatally by forming central, marginal, and subepithelial zones. Importantly, a large number of proliferating B cells and apoptotic cells are found in porcine IPPs postnatally, but not prenatally. The expression level of IgM in proliferating B cells depends on the zone in which distinct B cells are separately localized after birth. Specifically, IgM+ cells are predominantly found in the central zone, whereas IgM-/low cells are abundant in the marginal zone. Importantly, the cellular feature of IPPs differs from that of mesenteric lymph nodes (MLNs) where such distinct zones are not formed both prenatally and postnatally. Our findings suggest that IPPs (not MLNs) in postnatal pigs are involved in complementing functions of the primary lymphoid tissue that promotes the differentiation and maturation of B cells.
KW - B cells
KW - Peyer's patches
KW - ileum
KW - organogenesis
KW - pigs
UR - http://www.scopus.com/inward/record.url?scp=85097835795&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85097835795&partnerID=8YFLogxK
U2 - 10.3389/fimmu.2020.604674
DO - 10.3389/fimmu.2020.604674
M3 - Article
C2 - 33424851
AN - SCOPUS:85097835795
SN - 1664-3224
VL - 11
JO - Frontiers in Immunology
JF - Frontiers in Immunology
M1 - 604674
ER -