Glutamine-Induced Secretion of Intestinal Secretory Immunoglobulin A: A Mechanistic Perspective

Overview

Journal Front Immunol

Specialty Allergy & Immunology

Date 2016 Dec 10

PMID 27933057

Citations 29

Authors

Wenkai Ren

Kai Wang

Jie Yin

Shuai Chen

Gang Liu

Bie Tan

Guoyao Wu

Fuller W Bazer

Yuanyi Peng

Yulong Yin

Affiliations

Soon will be listed here.

Abstract

Secretory immunoglobulin A (SIgA) is one important line of defense in the intestinal mucosal surface to protect the intestinal epithelium from enteric toxins and pathogenic microorganisms. Multiple factors, such as intestinal microbiota, intestinal cytokines, and nutrients are highly involved in production of SIgA in the intestine. Recently, glutamine has been shown to affect intestinal SIgA production; however, the underlying mechanism by which glutamine stimulates secretion of intestinal SIgA is unknown. Here, we review current knowledge regarding glutamine in intestinal immunity and show that glutamine-enhanced secretion of SIgA in the intestine may involve intestinal microbiota, intestinal antigen sampling and presentation, induction pathways for SIgA production by plasma cells (both T-dependent and T-independent pathway), and even transport of SIgA. Altogether, the glutamine-intestinal SIgA axis has broad therapeutic implications for intestinal SIgA-associated diseases, such as celiac disease, allergies, and inflammatory bowel disease.

Citing Articles

Rejuvenating the gut: young plasma therapy improves cell proliferation, IGF-I and IGF-IR expression, and immune defense in aged male rats jejunum.

Asmaz E, Tan M, Genc A, Teker H, Ceylani T Biogerontology. 2025; 26(2):62.

PMID: 39969630 PMC: 11839702. DOI: 10.1007/s10522-025-10204-3.

Deciphering Pectin: A Comprehensive Overview of Its Origins, Processing, and Promising Utility.

Dang G, Li J, Yin C, Wang W, Zhang K, Zhong R ACS Omega. 2025; 10(1):1-15.

PMID: 39829568 PMC: 11740133. DOI: 10.1021/acsomega.4c01843.

Salivary assessment of the immune/inflammatory responses and oxidative stress in older adults vaccinated with CoronaVac or ChadOx-1.

Vieira J, de Oliveira T, Queiroz L, Camargo C, Nardy A, Monteiro F BMC Geriatr. 2024; 24(1):807.

PMID: 39363197 PMC: 11448442. DOI: 10.1186/s12877-024-05357-8.

Effects of γ-Aminobutyric Acid on Growth Performance, Immunity, Antioxidant Capacity, and Intestinal Microbiota of Growing Minks.

Li Y, Zhen S, Sun F, Cao L, Wang L Vet Sci. 2024; 11(9).

PMID: 39330777 PMC: 11435872. DOI: 10.3390/vetsci11090398.

Maternal resveratrol improves the intestinal health and weight gain of suckling piglets during high summer temperatures: The involvement of exosome-derived microRNAs and immunoglobin in colostrum.

Hong C, Huang Y, Yang G, Wen X, Wang L, Yang X Anim Nutr. 2024; 17:36-48.

PMID: 38464951 PMC: 10921242. DOI: 10.1016/j.aninu.2024.01.002.

References

Takechi H, Mawatari K, Harada N, Nakaya Y, Asakura M, Aihara M . Glutamine protects the small intestinal mucosa in anticancer drug-induced rat enteritis model. J Med Invest. 2014; 61(1-2):59-64. DOI: 10.2152/jmi.61.59. View

Farache J, Koren I, Milo I, Gurevich I, Kim K, Zigmond E . Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity. 2013; 38(3):581-95. PMC: 4115273. DOI: 10.1016/j.immuni.2013.01.009. View

Kruglov A, Grivennikov S, Kuprash D, Winsauer C, Prepens S, Seleznik G . Nonredundant function of soluble LTα3 produced by innate lymphoid cells in intestinal homeostasis. Science. 2013; 342(6163):1243-6. DOI: 10.1126/science.1243364. View

Ren W, Liu S, Chen S, Zhang F, Li N, Yin J . Dietary L-glutamine supplementation increases Pasteurella multocida burden and the expression of its major virulence factors in mice. Amino Acids. 2013; 45(4):947-55. DOI: 10.1007/s00726-013-1551-8. View

Mantis N, Rol N, Corthesy B . Secretory IgA's complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 2011; 4(6):603-11. PMC: 3774538. DOI: 10.1038/mi.2011.41. View

Vetizou M, Pitt J, Daillere R, Lepage P, Waldschmitt N, Flament C . Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 2015; 350(6264):1079-84. PMC: 4721659. DOI: 10.1126/science.aad1329. View

Yang H, Liu A, Zhang M, Ibrahim S, Pang Z, Leng X . Oral administration of live Bifidobacterium substrains isolated from centenarians enhances intestinal function in mice. Curr Microbiol. 2009; 59(4):439-45. DOI: 10.1007/s00284-009-9457-0. View

Ren W, Yin J, Wu M, Liu G, Yang G, Xion Y . Serum amino acids profile and the beneficial effects of L-arginine or L-glutamine supplementation in dextran sulfate sodium colitis. PLoS One. 2014; 9(2):e88335. PMC: 3914992. DOI: 10.1371/journal.pone.0088335. View

Smits H, Gloudemans A, van Nimwegen M, Willart M, Soullie T, Muskens F . Cholera toxin B suppresses allergic inflammation through induction of secretory IgA. Mucosal Immunol. 2009; 2(4):331-9. DOI: 10.1038/mi.2009.16. View

10.

Li Y, Chen Y, Zhang J, Zhu J, Liu Z, Liang S . Protective effect of glutamine-enriched early enteral nutrition on intestinal mucosal barrier injury after liver transplantation in rats. Am J Surg. 2010; 199(1):35-42. DOI: 10.1016/j.amjsurg.2008.11.039. View

11.

Dai Z, Wu G, Zhu W . Amino acid metabolism in intestinal bacteria: links between gut ecology and host health. Front Biosci (Landmark Ed). 2011; 16(5):1768-86. DOI: 10.2741/3820. View

12.

Corthesy B . Role of secretory IgA in infection and maintenance of homeostasis. Autoimmun Rev. 2012; 12(6):661-5. DOI: 10.1016/j.autrev.2012.10.012. View

13.

Johansen F, Kaetzel C . Regulation of the polymeric immunoglobulin receptor and IgA transport: new advances in environmental factors that stimulate pIgR expression and its role in mucosal immunity. Mucosal Immunol. 2011; 4(6):598-602. PMC: 3196803. DOI: 10.1038/mi.2011.37. View

14.

Tormo Carnicer R, Infante Pina D, Rosello Mayans E, Bartolome Comas R . [Intake of fermented milk containing Lactobacillus casei DN-114 001 and its effect on gut flora]. An Pediatr (Barc). 2006; 65(5):448-53. DOI: 10.1157/13094251. View

15.

Takenouchi-Ohkubo N, Asano M, Chihaya H, Chung-Hsuing W, Ishikasa K, Moro I . Retinoic acid enhances the gene expression of human polymeric immunoglobulin receptor (pIgR) by TNF-alpha. Clin Exp Immunol. 2004; 135(3):448-54. PMC: 1808977. DOI: 10.1111/j.1365-2249.2004.02398.x. View

16.

Lee I, Evans A, Yang C, Works M, Kumar V, De Miguel Z . Toxoplasma gondii is dependent on glutamine and alters migratory profile of infected host bone marrow derived immune cells through SNAT2 and CXCR4 pathways. PLoS One. 2014; 9(10):e109803. PMC: 4192591. DOI: 10.1371/journal.pone.0109803. View

17.

Yoshida M, Kobayashi K, Kuo T, Bry L, Glickman J, Claypool S . Neonatal Fc receptor for IgG regulates mucosal immune responses to luminal bacteria. J Clin Invest. 2006; 116(8):2142-2151. PMC: 1501111. DOI: 10.1172/JCI27821. View

18.

Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss C, Maza O . Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature. 2014; 514(7521):181-6. DOI: 10.1038/nature13793. View

19.

Fukatsu K, Kudsk K, Zarzaur B, Wu Y, Hanna M, DeWitt R . TPN decreases IL-4 and IL-10 mRNA expression in lipopolysaccharide stimulated intestinal lamina propria cells but glutamine supplementation preserves the expression. Shock. 2001; 15(4):318-22. DOI: 10.1097/00024382-200115040-00012. View

20.

Zhang X, Jiang X . Effects of enteral nutrition on the barrier function of the intestinal mucosa and dopamine receptor expression in rats with traumatic brain injury. JPEN J Parenter Enteral Nutr. 2013; 39(1):114-23. DOI: 10.1177/0148607113501881. View