Comprehensive Physiology Wiley Online Library

Immunophysiology of Intestinal Electrolyte Transport

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Effector Cells
1.1 Cells of Lamina Propria
1.2 Mast Cells
1.3 Phagocytes
2 Intermediate Targets
2.1 Amplification of Signal
2.2 Suppression of Signal
3 Soluble Mediators of Inflammation and Gut Response
3.1 Interleukins
3.2 Adenosine
3.3 Serotonin
3.4 Histamine
3.5 Kinins
3.6 Reactive Oxygen Metabolites
3.7 Platelet‐Activating Factor
3.8 Arachidonic Acid Metabolites
4 Neuroendocrine‐Immune Systems Interactions
4.1 Central Nervous System–Endocrine‐Immune Systems Interactions
4.2 Enteric Nervous System–Immune System Interactions
5 Integrated Responses to Immune System Stimulation
5.1 Mast Cell Activation (Gut Anaphylaxis)
5.2 Phagocyte Activation (Acute Inflammation)
6 Summary and Conclusions
Figure 1. Figure 1.

Mucosal mast cell activation and secretion. Mast cell progenitors under influence of interleukin 3 (IL‐3) differentiate into mucosal mast cells. When high‐affinity receptors on mast cell surface are occupied by immunoglobulin E (IgE) and then adjacent receptors are cross‐linked by antigen reacting with IgE, the mast cell is activated and degranulates. Both preformed products and newly synthesized mediators are secreted. PGD2, prostaglandin D2; LTB4, leukotriene B4; PAF, platelet‐activating factor.

Figure 2. Figure 2.

Phagocyte activation and secretion. Three categories of phagocytes—eosinophils, neutrophils, and macrophages—respond to soluble mediators or to phagocytosis of particles (microorganisms or cell debris) with chemotaxis and/or degranulation and secretion. Products of phagocyte secretion may amplify inflammatory signal or may have effects on other target cells in intestine such as enterocyte or muscularis. TNF, tumor necrosis factor; INF‐γ, interferon‐γ.

Figure 3. Figure 3.

Potential interactions between immune cells (macrophage) and mesenchymal cells (endothelium and fibroblasts). Mesenchymal cells and mast cells have receptors for IL‐1 and bradykinin that initiate prostaglandin synthesis and secretion.

Figure 4. Figure 4.

Subepithelial fibroblastic sheath of rabbit jejunal crypt. Fibroblasts (F) and fibroblast processes (FP) are separated from epithelial cells (E) by basement membrane. In region of crypts, these fibroblasts overlap, much like shingles on a roof. However, they extend beneath epithelial layer throughout intestine. Recent studies show that these are really myofibroblasts with contractile capabilities and that they are organized in a three‐dimensional network throughout intestinal lamina propria.

[From Parker et al. .]
Figure 5. Figure 5.

T cells are activated by macrophages when the macrophage presents antigen and secretes IL‐1. The T cell then elaborates a host of other lymphokines, particularly IL‐2, which cause clonal expansion of various lymphocyte lines to form classes of mature T cells and antibody‐producing plasma cells.

[From Fauci et al. .]
Figure 6. Figure 6.

Intestinal kallikrein‐kinin system. Activated tissue kallikrein acts on kininogens, synthesized and secreted by liver, to form a decapeptide, kallidin (LBK). Lysine is cleaved from LBK by an aminopeptidase to form bradykinin (BK). BK and LBK initiate intestinal secretion by releasing eicosanoids from lamina propria and also by receptor (and Ca2+)‐mediated, direct stimulation of enterocyte.

[From Powell . In: Physiology of the Gastrointestinal Tract (2nd ed.), © 1987, Raven Press, New York.]
Figure 7. Figure 7.

Sources and metabolism of reactive oxygen metabolites in gastrointestinal tract. Most important source is respiratory burst from phagocytic cells that secrete superoxide (O2·). O2· is rapidly metabolized by superoxide dismutase (SOD) to H2O2. H2O2 may be metabolized to H2O by 2 major oxidant defenses—catalase or glutathione peroxidase. Alternatively, H2O2 may be metabolized to hydroxyl (OH·) in the presence of Fe3+ by Haber‐Weiss reaction or it may be changed to hypohalous acids (HOX) by myeloperoxidase. These various oxidants—O2·, H2O2, OH·, and HOX—may induce tissue injury but may also take part in tissue defense by killing microorganisms and initiating intestinal water and electrolyte secretion to wash them from intestine.

[From Granger et al. .]
Figure 8. Figure 8.

Short‐circuit current response (Δ ISC) to reactive oxygen metabolites created by xanthine (X)/xanthine oxidase (XO) reaction in rabbit colon. There is a biphasic response that is inhibited by tetrodotoxin (TTX, 10−7 M) and by indomethacin (INDO, 10−6 M).

[From Bern et al. .]
Figure 9. Figure 9.

Biosynthetic pathway for platelet‐activating factor (AGEPC). In stimulated inflammatory cells, activated phospholipases remove arachidonic acid from ether phosphorylcholines (deacylation) to form lyso‐platelet‐activating factor (PAF). Acetyltransferases in presence of Ca2+ esterify an acetyl group (reacetylation) at sn‐2 position of glycerol to form PAF (AGEPC). AGEPC is then either secreted (also a Ca2+ ‐mediated process) where it binds to albumin for circulation in plasma or it binds to target cells. Degradation of PAF occurs by an acetylhydrolase that converts PAF to lyso‐PAF. It is important to note that activation of phospholipase A2 in inflammatory cell produces not only PAF but also arachidonic acid for further metabolism into bioactive eicosanoids.

[From Pinckard et al. . In: Inflammation: Basic Principles and Clinical Correlates, © 1988, Raven Press, New York.]
Figure 10. Figure 10.

Short‐circuit current response (Δ ISC) of rat colon to PAF (10 μM). PAF causes biphasic response that is inhibited by tetrodotoxin (TTX, 10−7 M) and indomethacin (INDO, 10−6 M).

[From Bern et al. .]
Figure 11. Figure 11.

Eicosanoid formation from tissue phospholipids. PLA2 and PLC, phospholipase A2 and C, respectively; HPETE, hydroperoxyeicosatetraenoic acid; HETE, hydroxyeicosatetraenoic acid; LT, leukotriene; N‐AcLTE4, N‐acetyl‐LTE4; LX, lipoxin; epoxy, epoxides; PG, prostaglandin; TX, thromboxane.

[From Feuerstein and Hallenbeck .]
Figure 12. Figure 12.

Biochemistry of arachidonic acid.

Figure 13. Figure 13.

Pathways for phospholipid metabolism and arachidonic acid formation in mammalian cells. Arachidonic acid can be freed from membrane phospholipids by the activity of either phospholipase C (PLase C) or phospholipase A2 (PLase A2). PLase C is receptor controlled, and it has been suggested recently that PLase A2 may be also. An additional enzyme, glyceride lipase, is necessary to free arachidonic acid from diacylglycerol (DG) that has been formed by PLase C metabolism of phosphoinositol (PI). IP3, inositol trisphosphate.

[From Powell et al. .]
Figure 14. Figure 14.

Proposed scheme for immune system regulation of intestinal electrolyte transport. Soluble mediators of inflammation such as histamine (HIST), PG, LT, PAF, H2O2, or unknown arachidonic acid metabolites (AA METAB) may directly stimulate epithelial cells, may stimulate mesenchymal cells such as endothelium and fibroblasts to produce more inflammatory mediators, or may modulate activity of enteric nervous system causing release of neurotransmitters. End result is inhibition of neutral NaCl absorption and stimulation of electrogenic Cl secretion by intestinal epithelium. Ach, acetylcholine; VIP, vasoactive intestinal polypeptide; EOS, eosinophils; PMN, polymorphonuclear neutrophil.

Figure 15. Figure 15.

Summary diagram of various systems controlling intestinal water and electrolyte transport. On left side of this colonic crypt are shown conventional controlling systems: bacteria, which elaborate heat labile (LT) and heat stable (ST) enterotoxins capable of initiating Cl secretion; endocrine system, an example of which is aldosterone, which changes mechanisms of Na absorption by colonic surface epithelium, augmenting its absorptive capacity; paracrine system, a part of enteric nervous system from which mucosal endocrine cells secrete either secretory (5‐HT) or absorptive (somatostatin) hormones directly onto adjacent epithelial cells; neural elements of enteric nervous system, which may have either secretory or absorptive effects. On right side is proposed new controlling element, the immune system. Immune cells (phagocytes, mast cells, and lymphocytes) and mesenchymal cells (endothelium, fibroblasts, and smooth muscle) release a host of soluble mediators such as PGE2 and PGI2, TXA2, HPETEs, LTs, adenosine (aden), histamine (hist), and serotonin (5‐HT). Because there are receptors for inflammatory mediators on endocrine cells and nerves and because there are receptors on immune cells for neurotransmitters and hormones, there is close communication and interaction between these various elements as they regulate intestinal water and electrolyte transport.



Figure 1.

Mucosal mast cell activation and secretion. Mast cell progenitors under influence of interleukin 3 (IL‐3) differentiate into mucosal mast cells. When high‐affinity receptors on mast cell surface are occupied by immunoglobulin E (IgE) and then adjacent receptors are cross‐linked by antigen reacting with IgE, the mast cell is activated and degranulates. Both preformed products and newly synthesized mediators are secreted. PGD2, prostaglandin D2; LTB4, leukotriene B4; PAF, platelet‐activating factor.



Figure 2.

Phagocyte activation and secretion. Three categories of phagocytes—eosinophils, neutrophils, and macrophages—respond to soluble mediators or to phagocytosis of particles (microorganisms or cell debris) with chemotaxis and/or degranulation and secretion. Products of phagocyte secretion may amplify inflammatory signal or may have effects on other target cells in intestine such as enterocyte or muscularis. TNF, tumor necrosis factor; INF‐γ, interferon‐γ.



Figure 3.

Potential interactions between immune cells (macrophage) and mesenchymal cells (endothelium and fibroblasts). Mesenchymal cells and mast cells have receptors for IL‐1 and bradykinin that initiate prostaglandin synthesis and secretion.



Figure 4.

Subepithelial fibroblastic sheath of rabbit jejunal crypt. Fibroblasts (F) and fibroblast processes (FP) are separated from epithelial cells (E) by basement membrane. In region of crypts, these fibroblasts overlap, much like shingles on a roof. However, they extend beneath epithelial layer throughout intestine. Recent studies show that these are really myofibroblasts with contractile capabilities and that they are organized in a three‐dimensional network throughout intestinal lamina propria.

[From Parker et al. .]


Figure 5.

T cells are activated by macrophages when the macrophage presents antigen and secretes IL‐1. The T cell then elaborates a host of other lymphokines, particularly IL‐2, which cause clonal expansion of various lymphocyte lines to form classes of mature T cells and antibody‐producing plasma cells.

[From Fauci et al. .]


Figure 6.

Intestinal kallikrein‐kinin system. Activated tissue kallikrein acts on kininogens, synthesized and secreted by liver, to form a decapeptide, kallidin (LBK). Lysine is cleaved from LBK by an aminopeptidase to form bradykinin (BK). BK and LBK initiate intestinal secretion by releasing eicosanoids from lamina propria and also by receptor (and Ca2+)‐mediated, direct stimulation of enterocyte.

[From Powell . In: Physiology of the Gastrointestinal Tract (2nd ed.), © 1987, Raven Press, New York.]


Figure 7.

Sources and metabolism of reactive oxygen metabolites in gastrointestinal tract. Most important source is respiratory burst from phagocytic cells that secrete superoxide (O2·). O2· is rapidly metabolized by superoxide dismutase (SOD) to H2O2. H2O2 may be metabolized to H2O by 2 major oxidant defenses—catalase or glutathione peroxidase. Alternatively, H2O2 may be metabolized to hydroxyl (OH·) in the presence of Fe3+ by Haber‐Weiss reaction or it may be changed to hypohalous acids (HOX) by myeloperoxidase. These various oxidants—O2·, H2O2, OH·, and HOX—may induce tissue injury but may also take part in tissue defense by killing microorganisms and initiating intestinal water and electrolyte secretion to wash them from intestine.

[From Granger et al. .]


Figure 8.

Short‐circuit current response (Δ ISC) to reactive oxygen metabolites created by xanthine (X)/xanthine oxidase (XO) reaction in rabbit colon. There is a biphasic response that is inhibited by tetrodotoxin (TTX, 10−7 M) and by indomethacin (INDO, 10−6 M).

[From Bern et al. .]


Figure 9.

Biosynthetic pathway for platelet‐activating factor (AGEPC). In stimulated inflammatory cells, activated phospholipases remove arachidonic acid from ether phosphorylcholines (deacylation) to form lyso‐platelet‐activating factor (PAF). Acetyltransferases in presence of Ca2+ esterify an acetyl group (reacetylation) at sn‐2 position of glycerol to form PAF (AGEPC). AGEPC is then either secreted (also a Ca2+ ‐mediated process) where it binds to albumin for circulation in plasma or it binds to target cells. Degradation of PAF occurs by an acetylhydrolase that converts PAF to lyso‐PAF. It is important to note that activation of phospholipase A2 in inflammatory cell produces not only PAF but also arachidonic acid for further metabolism into bioactive eicosanoids.

[From Pinckard et al. . In: Inflammation: Basic Principles and Clinical Correlates, © 1988, Raven Press, New York.]


Figure 10.

Short‐circuit current response (Δ ISC) of rat colon to PAF (10 μM). PAF causes biphasic response that is inhibited by tetrodotoxin (TTX, 10−7 M) and indomethacin (INDO, 10−6 M).

[From Bern et al. .]


Figure 11.

Eicosanoid formation from tissue phospholipids. PLA2 and PLC, phospholipase A2 and C, respectively; HPETE, hydroperoxyeicosatetraenoic acid; HETE, hydroxyeicosatetraenoic acid; LT, leukotriene; N‐AcLTE4, N‐acetyl‐LTE4; LX, lipoxin; epoxy, epoxides; PG, prostaglandin; TX, thromboxane.

[From Feuerstein and Hallenbeck .]


Figure 12.

Biochemistry of arachidonic acid.



Figure 13.

Pathways for phospholipid metabolism and arachidonic acid formation in mammalian cells. Arachidonic acid can be freed from membrane phospholipids by the activity of either phospholipase C (PLase C) or phospholipase A2 (PLase A2). PLase C is receptor controlled, and it has been suggested recently that PLase A2 may be also. An additional enzyme, glyceride lipase, is necessary to free arachidonic acid from diacylglycerol (DG) that has been formed by PLase C metabolism of phosphoinositol (PI). IP3, inositol trisphosphate.

[From Powell et al. .]


Figure 14.

Proposed scheme for immune system regulation of intestinal electrolyte transport. Soluble mediators of inflammation such as histamine (HIST), PG, LT, PAF, H2O2, or unknown arachidonic acid metabolites (AA METAB) may directly stimulate epithelial cells, may stimulate mesenchymal cells such as endothelium and fibroblasts to produce more inflammatory mediators, or may modulate activity of enteric nervous system causing release of neurotransmitters. End result is inhibition of neutral NaCl absorption and stimulation of electrogenic Cl secretion by intestinal epithelium. Ach, acetylcholine; VIP, vasoactive intestinal polypeptide; EOS, eosinophils; PMN, polymorphonuclear neutrophil.



Figure 15.

Summary diagram of various systems controlling intestinal water and electrolyte transport. On left side of this colonic crypt are shown conventional controlling systems: bacteria, which elaborate heat labile (LT) and heat stable (ST) enterotoxins capable of initiating Cl secretion; endocrine system, an example of which is aldosterone, which changes mechanisms of Na absorption by colonic surface epithelium, augmenting its absorptive capacity; paracrine system, a part of enteric nervous system from which mucosal endocrine cells secrete either secretory (5‐HT) or absorptive (somatostatin) hormones directly onto adjacent epithelial cells; neural elements of enteric nervous system, which may have either secretory or absorptive effects. On right side is proposed new controlling element, the immune system. Immune cells (phagocytes, mast cells, and lymphocytes) and mesenchymal cells (endothelium, fibroblasts, and smooth muscle) release a host of soluble mediators such as PGE2 and PGI2, TXA2, HPETEs, LTs, adenosine (aden), histamine (hist), and serotonin (5‐HT). Because there are receptors for inflammatory mediators on endocrine cells and nerves and because there are receptors on immune cells for neurotransmitters and hormones, there is close communication and interaction between these various elements as they regulate intestinal water and electrolyte transport.

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D. W. Powell. Immunophysiology of Intestinal Electrolyte Transport. Compr Physiol 2011, Supplement 19: Handbook of Physiology, The Gastrointestinal System, Intestinal Absorption and Secretion: 591-641. First published in print 1991. doi: 10.1002/cphy.cp060425