Timing, Localization, and Persistence of Colonization by Segmented Filamentous Bacteria in the Neonatal Mouse Gut Depend on Immune Status of Mothers and Pups

ABSTRACT As a member of the indigenous gut mucosal microbiota, segmented filamentous bacteria (SFB) colonize the guts of a variety of vertebrates and invertebrates. They are potent microbial stimuli of the gut mucosal immune system. In the small intestines of mice and rats, it has been observed that SFB are absent during the suckling period and appear in high numbers shortly after weaning, then quickly retreat to the cecum and large intestine. In this study, we explored whether this microecological phenomenon resulted from the interaction between SFB and the passively acquired maternal mucosal immunity and/or the actively acquired mucosal immunity. We set up a mouse model by reciprocal crossings and backcrossings of SFB-monoassociated, formerly germ-free, immunocompetent (+/+) BALB/c mice and immunodeficient (scid/scid) mice to produce pups which are either immunocompetent (scid/+) or immunodeficient (scid/scid) and are born either to immunocompetent (scid/+) mothers or to immunodeficient (scid/scid) mothers. We monitored the number of SFB on the mucosa of the small intestine in the four different groups of mice after birth, as well as the level of passively acquired antibodies, the active gut mucosal immune responses, and immunoglobulin A (IgA) coating of SFB in the gut. The results showed that, irrespective of whether the pups were scid/scid or scid/+, SFB could be found earlier on the mucosa of the small intestine in pups born to scid/scid mothers, appearing from day 13 and rapidly reaching a climax around weaning time on day 28, compared to the significantly delayed colonization in the pups of scid/+ mothers, starting from day 16 and peaking around days 28 to 32. After the climax, SFB quickly declined to very low levels in the small intestines of scid/+ pups of either scid/scid mothers or scid/+ mothers, whereas they remained at high levels in scid/scid pups at least until day 70, the last observation time in this study. The dynamic changes in SFB colonization of the small intestines of the different groups of pups may be related to the dynamic changes in the levels of SFB coated with secretory IgA (sIgA), which resulted from the significantly different levels of sIgA obtained from the mothers' milk during the suckling period and, later, of self-produced sIgA in the small intestine. Nevertheless, it is evident that the timing, localization, and persistence of colonization of the neonatal gut by SFB depends on the immune status of both mothers and pups.

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Segmented filamentous bacteria in the rodent small intestine: Their colonization of growing animals and possible role in host resistance toSalmonella

Microbial Ecology ◽

10.1007/bf02010451 ◽

1982 ◽

Vol 8 (2) ◽

pp. 181-190 ◽

Cited By ~ 56

Author(s):

Christian D. Garland ◽

Adrian Lee ◽

Melvyn R. Dickson

Keyword(s):

Small Intestine ◽

Host Resistance ◽

Filamentous Bacteria ◽

Segmented Filamentous Bacteria

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Comparison of the Small Intestine of 0-day-old Neonatal Piglets vs. 21-day-old Weaned Piglets

10.21203/rs.3.rs-26152/v1 ◽

2020 ◽

Author(s):

Chen Yuan ◽

Yuxin Jin ◽

Abid Ullah Shah ◽

En Zhang ◽

penghao Zhang ◽

...

Keyword(s):

Small Intestine ◽

Immune Cells ◽

Secretory Iga ◽

Secretory Cells ◽

Weaned Piglets ◽

Neonatal Piglets ◽

Weaned Piglet ◽

Small Intestines ◽

Mechanistic Basis

Abstract Background: Neonatal piglets are susceptible to intestinal infections . Gut is the body’s major immune structure and the intestinal mucosa, which is composed of intestinal epithelial cells (IELs) and subepithelial natural immune cells, is considered as the primary site for eliciting local immune responses to foreign antigens. This study compared the intestinal immune cells of neonatal and weaned piglets to provide a theoretical and mechanistic basis for preventing intestinal infectious diseases. Results: Histological analyses of weaned piglet intestines showed increased crypt depth, high IEL count, and increased areas of ileal Peyer’s patches. Additionally, the duodenal and ileal villi of weaned piglets were longer than those of neonatal piglets. Expression of claudin-3 protein in weaned piglets was remarkably high as compared with neonatal piglets. The number of CD3 + T cells, goblet cells, and secretory cells was high in the small intestines of weaned piglets in vivo. Contrarily, secretory IgA-positive cell numbers in the jejunum remained unchanged between neonatal and weaned piglets. Gene expression of 12 pattern recognition receptor (PRR) (TLR1–10, MDA5, and RIG-I) was examined in neonatal and weaned piglet small intestine (duodenum, jejunum , and ileum). The pattern of mRNA expression level of most PRR genes in the duodenum and jejunum was inverse of that in the ileum. Compared with weaned piglets, there were significantly fewer intestinal lymphocytes at birth in neonatal pigs. Conclusions: The physical, biochemical, and immune-related components of neonatal and weaned piglet small intestines were investigated to provide preliminary data on the pathogenetic mechanism for future studies.

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Interactions between gut-associated lymphoid tissue and colonization levels of indigenous, segmented, filamentous bacteria in the small intestine of mice

Canadian Journal of Microbiology ◽

10.1139/w98-122 ◽

1998 ◽

Vol 44 (12) ◽

pp. 1177-1182 ◽

Cited By ~ 26

Author(s):

J Snel ◽

C C Hermsen ◽

H J Smits ◽

N A Bos ◽

WMC Eling ◽

...

Keyword(s):

Small Intestine ◽

Immune System ◽

Lymphoid Tissue ◽

Immune Reaction ◽

Mucosal Immune System ◽

Filamentous Bacteria ◽

Segmented Filamentous Bacteria ◽

Swiss Mice ◽

Age Dependent ◽

Old Mice

Unlike most other indigenous bacteria, segmented filamentous bacteria (SFB) are potent activators of the mucosal immune system. SFB are strongly anchored to the epithelial cells of the small intestine where they have a preference for mucosal lymphoid epithelium. Since SFB are only present in high numbers shortly after weaning, it was investigated whether an SFB-induced immune reaction results in the removal of these bacteria from the small intestine. A correlation was found between age and colonization levels in the small intestines of SFB monoassociated Swiss mice. Five-week-old athymic BALB/c (nu/nu) mice showed lower colonization levels than their heterozygous littermates, but the opposite was found at the age of 12 weeks. However, SFB inoculation of germfree Swiss mice resulted in higher colonization levels in 5-week-old mice when compared with 4-month-old mice. We conclude that SFB colonization levels in the small intestine are likely influenced by the activity of the mucosal immune system. However, an additional age-dependent factor that modulates SFB colonization levels cannot be excluded.Key words: segmented filamentous bacteria, small intestine, gut-associated lymphoid tissue.

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Single-blinded Study Highlighting the Differences between the Small Intestines of Neonatal and Weaned Piglets

10.21203/rs.3.rs-26152/v2 ◽

2020 ◽

Author(s):

Chen Yuan ◽

Yuxin Jin ◽

Abid Ullah Shah ◽

En Zhang ◽

penghao Zhang ◽

...

Keyword(s):

Pattern Recognition ◽

T Cells ◽

Small Intestine ◽

Mononuclear Cells ◽

Pattern Recognition Receptors ◽

Secretory Iga ◽

Secretory Cells ◽

Weaned Piglets ◽

Neonatal Piglets ◽

Small Intestines

Abstract Background: The gut is the body’s major immune structure, and the gut mucosa, which contains intraepithelial lymphocytes (IELs) and subepithelial natural immune cells, is considered the primary site for eliciting local immune responses to foreign antigens. Pigs are susceptible to intestinal infections at all life stages; however, neonates tend to be the most susceptible. This study compared the small intestine of neonatal and weaned piglets to provide a theoretical basis for preventing intestinal infectious diseases in neonatal piglets. Results: Histological analyses of weaned piglet intestines showed increased crypt depth, higher IEL count, and larger ileal Peyer’s patches compared with those of neonates. Additionally, the ileal villi of weaned piglets were longer than those of neonatal piglets. The expression of claudin-3 and occludin protein was remarkably higher in weaned piglets than in neonatal piglets. The numbers of CD3 + T cells, goblet cells, and secretory cells were also higher in the small intestine of weaned piglets than in those of neonates. The number of secretory IgA-positive cells in the jejunum was not significantly different between neonatal and weaned piglets. The gene expression of 12 pattern recognition receptors (PRRs), such as TLR1–10, MDA5, and RIG-I in the small intestines of both neonatal and weaned piglets was also examined. The mRNA expression of most pattern recognition receptors genes in the duodenum and jejunum was higher in weaners than in neonates; however, the inverse was true in the ileum. Compared with that in weaned piglets, there were significantly fewer CD3 + , CD4 + , and CD8 + T cells from peripheral blood-mononuclear cells in neonatal piglets. Conclusions: In this study, the physical and immunological components of small intestines of neonatal and weaned piglets were investigated. Our results provide preliminary data on differences in the immune mechanisms between the small intestines of 0- and 21-day-old piglets. Future studies could focus on additional developmental stages of pigs and how the differences in their small intestines affect the animal’s response to pathogens

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Influence of Diets Containing Native or BoiledPhaseolus vulgarison Segmented Filamentous Bacteria in the Small Intestine of Mice

Microbial Ecology in Health and Disease ◽

10.3402/mehd.v4i3.7652 ◽

1991 ◽

Vol 4 (3) ◽

Author(s):

H. L. B. M. Klaasen ◽

J. P. Koopman ◽

M. E. Van Den Brink ◽

P. M. Scholten ◽

M. H. Bakker ◽

...

Keyword(s):

Small Intestine ◽

Filamentous Bacteria ◽

Segmented Filamentous Bacteria

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Influence of Macronutrients on Segmented Filamentous Bacteria in the Small Intestine of Mice

Microbial Ecology in Health and Disease ◽

10.3109/08910609109140263 ◽

1991 ◽

Vol 4 (1) ◽

pp. 47-51 ◽

Cited By ~ 4

Author(s):

H. L. B. M. Klaasen ◽

J. P. Koopman ◽

M. E. Van Den Brink ◽

P. M. Scholten ◽

A. C. Beynen

Keyword(s):

Small Intestine ◽

Filamentous Bacteria ◽

Segmented Filamentous Bacteria

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Differential Roles of Segmented Filamentous Bacteria and Clostridia in Development of the Intestinal Immune System

Infection and Immunity ◽

10.1128/iai.67.7.3504-3511.1999 ◽

1999 ◽

Vol 67 (7) ◽

pp. 3504-3511 ◽

Cited By ~ 169

Author(s):

Yoshinori Umesaki ◽

Hiromi Setoyama ◽

Satoshi Matsumoto ◽

Akemi Imaoka ◽

Kikuji Itoh

Keyword(s):

Small Intestine ◽

Immune System ◽

Large Intestine ◽

Immunoglobulin A ◽

Cell Receptor ◽

Intraepithelial Lymphocytes ◽

Filamentous Bacteria ◽

Segmented Filamentous Bacteria ◽

Intestinal Immune System ◽

Gnotobiotic Mice

ABSTRACT The presence of microflora in the digestive tract promotes the development of the intestinal immune system. In this study, to evaluate the roles of two types of indigenous microbe, segmented filamentous bacteria (SFB) and clostridia, whose habitats are the small and large intestines, respectively, in this immunological development, we analyzed three kinds of gnotobiotic mice contaminated with SFB, clostridia, and both SFB and clostridia, respectively, in comparison with germfree (GF) or conventionalized (Cvd) mice associated with specific-pathogen-free flora. In the small intestine, the number of αβ T-cell receptor-bearing intraepithelial lymphocytes (αβIEL) increased in SFB-associated mice (SFB-mice) but not in clostridium-associated mice (Clost-mice). There was no great difference in Vβ usage among GF mice, Cvd mice, and these gnotobiotic mice, although the association with SFB decreased the proportion of Vβ6+ cells in CD8β− subsets to some extent, compared to that in GF mice. The expression of major histocompatibility complex class II molecules on the epithelial cells was observed in SFB-mice but not in Clost-mice. On the other hand, in the large intestine, the ratio of the number of CD4−CD8+ cells to that of CD4+ CD8−cells in αβIEL increased in Clost-mice but not in SFB-mice. On association with both SFB and clostridia, the numbers and phenotypes of IEL in the small and large intestines changed to become similar to those in Cvd mice. In particular, the ratio of the number of CD8αβ+ cells to that of CD8αα+ cells in αβIEL, unusually elevated in the small intestines of SFB-mice, decreased to the level in Cvd mice on contamination with both SFB and clostridia. The number of immunoglobulin A (IgA)-producing cells in the lamina propria was more elevated in SFB-mice than in Clost-mice, not only in the ileum but also in the colon. The number of IgA-producing cells in the colons of Clost-mice was a little increased compared to that in GF mice. Taken together, SFB and clostridia promoted the development of both IEL and IgA-producing cells in the small intestine and that of only IEL in the large intestine, respectively, suggesting the occurrence of compartmentalization of the immunological responses to the indigenous bacteria between the small and large intestines.

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Scanning electron microscopic observations of segmented filamentous bacteria in the small intestine of domestic fowl

Veterinary Record ◽

10.1136/vr.111.16.366 ◽

1982 ◽

Vol 111 (16) ◽

pp. 366-367 ◽

Cited By ~ 9

Author(s):

G. Pearson ◽

M. McNulty ◽

R. McCracken ◽

W. Curran

Keyword(s):

Small Intestine ◽

Domestic Fowl ◽

Filamentous Bacteria ◽

Electron Microscopic ◽

Segmented Filamentous Bacteria ◽

Scanning Electron Microscopic ◽

Scanning Electron

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Segmented Filamentous Bacteria Interact with Intraepithelial Mononuclear Cells

Infection and Immunity ◽

10.1128/iai.70.6.3277-3280.2002 ◽

2002 ◽

Vol 70 (6) ◽

pp. 3277-3280 ◽

Cited By ~ 26

Author(s):

David K. Meyerholz ◽

Thomas J. Stabel ◽

Norman F. Cheville

Keyword(s):

Immune System ◽

Mucosal Immunity ◽

Mononuclear Cells ◽

Direct Interaction ◽

Filamentous Bacteria ◽

Segmented Filamentous Bacteria ◽

Multiple Species

ABSTRACT Segmented filamentous bacteria (SFB) are found in multiple species and play an important role in the development of mucosal immunity. The mechanism by which the bacteria interact with the immune system has not been well defined. We provide morphologic evidence of direct interaction between SFB and intraepithelial mononuclear cells.

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