Skip to main content

Intestinal epithelial function: The case for immunophysiological regulation

Implications for disease (second of two parts)

Abstract

Substantial amounts of data have been reported showing a role for immunomodulation of epithelial function (particularly ion secretion and permeability) using animal models of anaphylactic reactions. In part one of this review we outlined the main immune cell types and mediators/cytokines that are currently known to influence epithelial physiology either directly, or indirectly via an intermediate cell type. Here we will expand on the significance of these studies and show how antigenic activation of the mucosal immune system can evoke changes in epithelial function that may be beneficial to the host by mediating loss/inactivation of the antigen. However, a continued and inappropriate immune stimulation can lead to pathophysiological reactions and disease. Thus, we will present data on immune regulation of epithelial function with direct applicability to understanding the mechanism underlying human intestinal inflammatory and secretory disease. Finally, we highlight key strategic points in the cascade of immune events that can control epithelial function and thus may be of relevance in the formulation of new therapeutic approaches to intestinal inflammation.

This is a preview of subscription content, access via your institution.

References

  1. Stead RH, Tomioka M, Quinonez G, Simon GT, Felten SY, Bienenstock J: Intestinal mucosal mast cells in normal and nematode-infected rat intestines are in intimate contact with peptidergic nerves. Proc Natl Acad Sci USA 84:2975–2979, 1987

    Google Scholar 

  2. Archampong EQ, Harris J, Clark CG: The absorption and secretion of water and electrolytes across healthy and disease human colonic mucosa measuredin vitro. Gut 13:880–886, 1972

    Google Scholar 

  3. Barrett KE, Dharmasthaphorn K: Secretion and absorption: Small intestine and colon.In The Textbook of Gastroenterology. T Yamada (ed). Philadelphia, Lippincott, 1991, pp 265–294

    Google Scholar 

  4. Field M, Rao MC, Chang EB: Intestinal electrolyte transport and diarrheal disease. Parts 1 and 2. N Engl J Med 321:800–805, 879–883, 1989

    Google Scholar 

  5. Powell DW: The immunophysiology of intestinal electrolyte transport.In Absorptive and Secretory processes of the Intestine. Handbook of Physiology, The Gastrointestinal System IV. RA Fizzell, M Field (eds). Bethesda, American Physiology Society, 1991, pp 591–641

    Google Scholar 

  6. Goodlad RA: Gastrointestinal epithelial cell proliferation. Dig Dis 7:169–177, 1989

    Google Scholar 

  7. Cereijido M, Gonzalez-Mariscal L, Contreras G: Tight junction: Barrier between organisms and environment. News Physiol Sci 4:72–75, 1989

    Google Scholar 

  8. Cereijido M (ed): Tight Junctions. Boca Raton, CRC Press, 1992

    Google Scholar 

  9. Holmes R, Lobley RW: Intestinal brush border revisited. Gut 30:1667–1678, 1989

    Google Scholar 

  10. Holmes R: The intestinal brush border. Gut 12:668–677, 1971

    Google Scholar 

  11. Carne RK, Miller D, Bihler I: The restrictions on the possible mechanisms of intestinal transport of sugars.In Membrane Transport and Metabolism. A. Kleinzeller A Kotyk (eds). London, Academic Press, 1961, pp 434–350

    Google Scholar 

  12. Atisook K, Madara JL: An oligopeptide permeates intestinal tight junctions at glucose-elicited dilatations. Gastroenterology 100:719–724, 1991

    Google Scholar 

  13. Pappenheimer JR, Reiss KZ: Contribution of solvent drag through intercellular junctions to absorption of nutrients by the small intestine. J Membr Biol 100:123–136, 1987

    Google Scholar 

  14. Kagnoff MR: Immunology of the digestive system.In Physiology of the Gastrointestinal Tract, 1st ed. LR Johnston (ed). New York, Raven Press, 1981, pp 1337–1359

    Google Scholar 

  15. Naor D: A different outlook at the phenotype-function relationships of T cell subpopulations: Fundamental and clinical implications. Clin Immunol Immunopathol 62:127–132, 1992

    Google Scholar 

  16. Kiyono H, Taguchi T, Aicher WK, Beagley KW, Fujihashi K, Eldridge JH, McGhee JR: Immunoregulatory confluence: T cell, Fc Receptors and cytokines for IgA immune responses. Int Rev Immunol 6:263–273, 1990

    Google Scholar 

  17. Roitt I, Brostoff J, Male D: Immunology, 2nd ed. London, Churchill Livingstone, 1989

    Google Scholar 

  18. Brandtzaeg P, Sollid LM, Thrane PS, Kvale D, Bjerke K, Scott H, Kett K, Rognum TO: Lymphoepithelial interactions in the mucosal immune system. Gut 29:1116–1130, 1988

    Google Scholar 

  19. Croitoru K, Ernst PB: Leukocytes in the intestinal epithelium: An unusual immunological compartment revisited. Regional Immunol 4:63–69, 1992

    Google Scholar 

  20. Cerf-Bensussan N, Guy-Grand D: Intestinal intraepithelial lymphocytes. Gastroenterol Clin North Am 20:549–574, 1991

    Google Scholar 

  21. Arizono N, Nakao S: Kinetics and staining properties of mast cells proliferating in rat small intestine tuniva muscularis and subserosa following infection withNippostrongylus brasiliensis. APMIS 96:964–970, 1988

    Google Scholar 

  22. Befus AD, Fujimaki H, Lee TDG, Swieter M: Mast cell polymorphisms: Present concepts, future directions. Dig Dis Sci 33(suppl):16S-24S, 1988

    Google Scholar 

  23. Galli SJ, Gordon JR, Wershill BK: Cytokine production by mast cells and basophils. Curr Opin Immunol 3:865–873, 1991

    Google Scholar 

  24. Conrad DH, Squire CM, Bartlett WC, Dierks SE: Fc∈ receptors. Curr Opin Immunol 3:859–864, 1991

    Google Scholar 

  25. Gordon JR, Galli S: Release of both preformed and newly synthesised tumour necrosis factor α (TNFα)/cachectin by mouse mast cells stimulated via Fc∈RI. A mechanism for the sustained action of mast cell-derived TNFα during IgE-dependent biological responses. J Exp Med 174:103–107, 1991

    Google Scholar 

  26. Wershill BK, Galli SJ: Gastrointestinal mast cells. New approaches for analyzing their functionin vivo. Gastroenterol Clin North Am 20:613–627, 1991

    Google Scholar 

  27. Plaut M, Pierce JH, Watson CJ, Hankey-Hyde J, Nordan RP, Paul WE: Mast cell lines produce lymphokines in response to cross-linkage of Fc∈RI or to calcium ionophore. Nature 339:64–67, 1989

    Google Scholar 

  28. Shanahan F, Denburg J, Fox J, Bienenstock J: Mast cell heterogeneity: Effects of neuroenteric peptides on histamine release. J Immunol 135:1331–1337, 1985

    Google Scholar 

  29. Theoharides TC, Kops SK, Bondy PK, Askenase PW: Differential release of serotonin without comparable histamine under diverse conditions in the rat mast cell. Biochem Pharmacol 34:1389–1398, 1985

    Google Scholar 

  30. Capron A, Dessaint JP, Capron M, Joseph M, Ameisen JC, Tonnel AB: From parasites to allergy: A second receptor for IgE. Immunol Today 7:15–18, 1986

    Google Scholar 

  31. Nash S, Parkos C, Nusrat A, Delp C, Madara JL:In vitro model of intestinal crypt abscess. A novel neutrophil-derived secretagogue activity. J Clin Invest 87:1474–1477, 1991

    Google Scholar 

  32. von Ritter C, Be R, Granger DN: Neutrophilic proteases: Mediators of formyl-methionyl-leucyl-phenylalanine-induced ileitis in rats. Gastroenterology 97:605–609, 1989

    Google Scholar 

  33. Befus AD: Neuromodulation of gastrointestinal immune and inflammatory responses.In Immunopharmacology of the Gastrointestinal System. JL Wallace (ed.) London, Academic Press, 1993, pp 1–14

    Google Scholar 

  34. Ottaway CA: Neuroimmunomodulation in the intestinal mucosa. Gastroenterol Clin North Am 20:511–528, 1991

    Google Scholar 

  35. Cooke HJ: Role of the “little brain” in the gut in water and electrolyte homeostasis. FASEB J 3:127–139, 1989

    Google Scholar 

  36. Blalock JE: A molecular basis for bidirectional communication between the immune and the neuroendocrine system. Physiol Rev 69:1–32, 1989

    Google Scholar 

  37. Cheng H, Leblond CP: Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. III. Entero-endocrine cells. Am J Anat 141:503–520, 1974

    Google Scholar 

  38. Johnston CF, Bell PM, Collins BJ, Shaw C, Love AHG, Buchanan KD: Reassessment of enteric endocrine cell hyperplasia in celiac disease. Hepato-Gastroenterol 35:88–92, 1988

    Google Scholar 

  39. Lake AM, Bloch KL, Sinclair KJ, Walker WA: Anaphylactic release of intestinal mucus. Immunology 39:173–178, 1980

    Google Scholar 

  40. McKay DM, Halton DW, McCaigue MD, Johnston CF, Fairweather I, Shaw C:Hymenolepis diminuta: Intestinal goblet cell response to infection in male C57 mice. Exp Parasitol 71:9–20, 1990

    Google Scholar 

  41. Miller HRP, Nawa Y, Parish CR: Intestinal goblet cell differentiation inNippostrongylus-infected rats after transfer of fractionated thoracic duct lymphocytes. Int Arch Allergy Appl Immunol 59:281–285, 1979

    Google Scholar 

  42. Neutra MR, O'Malley LJ, Specian RD: Regulation of goblet cell secretion II. A survey of potential secretagogues. Am J Physiol 242:G380-G387, 1982

    Google Scholar 

  43. Tao P, Wilson DE: Effects of prostaglandin E2, 16,16-dimethyl prostaglandin E2 and a prostaglandin endoperoxide analogue (U-46619) on gastric acid secretory volume, [H+] and mucus synthesis and secretion in the rat. Prostaglandins 28:353–365, 1984

    Google Scholar 

  44. Berschneider HM, Powell DW: Fibroblasts modulate intestinal secretory responses to inflammatory mediators. J Clin Invest 89:484–489, 1992

    Google Scholar 

  45. Moore R, Carlson S, Madara JL: Villus contraction aids repair of intestinal epithelium after injury. Am J Physiol 257:G274-G283 1989

    Google Scholar 

  46. Schultz SG, Zalusky R: Ion transport in isolated rabbit ileum. I. Short-circuit current and Na fluxes. J Gen Physiol 47:567–584, 1964

    Google Scholar 

  47. Perdue MH, Gall, DG: Intestinal anaphylaxis in the rat: Jejunal response toin vitro antigen exposure. Am J Physiol 250:G427-G431, 1986

    Google Scholar 

  48. Bienenstock J, Befus AD: Some thoughts on the biologic role of immunoglobulin A. Gastroenterology 84:178–185, 1983

    Google Scholar 

  49. Yamada M, Nakazawa M, Kamata I, Arizono N: Low-level infection with the nematodeNippostrongylus brasiliensis induces significant and sustained specific and non-specific IgE antibody responses in rats. Immunology 75:36–40, 1992

    Google Scholar 

  50. Harari Y, Castro GA: Reconstitution of immune-mediated ion secretion in gut of the athymic rat. Parasite Immunol 13:313–328, 1991

    Google Scholar 

  51. Halpern GM, Scott JR: Non-IgE antibody mediated mechanisms in food allergy. Ann Allergy 58:14–27, 1987

    Google Scholar 

  52. Baird AW, Barclay WS, Blazer-Yost BL, Cuthbert AW: Affinity purified immunoglobulin G transfers immediate hypersensitivity to guinea pig colonic epitheliumin vitro. Gastroenterology 92:635–642, 1987

    Google Scholar 

  53. Rangachari PK: Histamine: Mercurial messenger in the gut. Am J Physiol 262:G1-G13, 1992

    Google Scholar 

  54. Beer DJ, Matloff SM, Rocklin RE: The influence of histamine on immune and inflammatory response. Adv Immunol 35:209–268, 1984

    Google Scholar 

  55. Haaksma EEJ, Leurs R, Timmerman H: Histamine receptors: Subclasses and specific ligands. Pharmacol Ther 47:73–104, 1990

    Google Scholar 

  56. Brandes LJ, Labella FS, Galvin GB, Paraskevas F, Saxena SP, McNicol A, Gerrard JM: Histamine as an intracellular messenger. Biochem Pharmacol 40:1677–1681, 1990

    Google Scholar 

  57. McCabe RD, Smith PL: Effects of histamine and histamine receptor antagonists on ion transport in rabbit transcending colon. Am J Physiol 247:G411-G418, 1984

    Google Scholar 

  58. Hardcastle J, Hardcastle PT: The secretory actions of histamine in rat small intestine. J Physiol (London) 388:521–532, 1987

    Google Scholar 

  59. Wassermann SI, Barrett KE, Huott PA, Beuerlein G, Kagnoff MF, Dharmsathaphorn K: Immune-related intestinal Cl secretion. I. Effect of histamine on the T84 cell line. Am J Physiol 254:C53-C62, 1988

    Google Scholar 

  60. Cohn JA, Dougherty NC, King WF: Histamine stimulates calcium-mediated protein phosphorylation in colonic epithelial cell line. Biochem Biophys Res Commun 165:810–816, 1989

    Google Scholar 

  61. Wang Y-Z, Cooke HJ: H2 receptors mediate cyclical chloride secretion in guinea pig distal colon. Am J Physiol 258:G887-G893, 1990

    Google Scholar 

  62. Wood JD: Communication between minibrain in the gut and enteric immune system. News Physiol Sci 6:359–364, 1991

    Google Scholar 

  63. Wang Y-Z, Cooke HJ, Su H-C, Fertel R: Histamine augments colonic secretion in guinea pig distal colon. Am J Physiol 258:G432-G439, 1990

    Google Scholar 

  64. Kuwahara A, Cooke HJ: Tachykinin induced anion secretion in guinea pig distal colon: Role of neural and inflammatory mediators. J Pharmacol Exp Ther 252:1–7, 1990

    Google Scholar 

  65. Beubler E, Bukhave K, Rask-Madsen J: Significance of calcium for the prostaglandin E2-mediated secretory response to 5-hydroxytryptamine in the small intestine of the ratin vivo. Gastroenterology 90:1972–1977, 1986

    Google Scholar 

  66. Zimmerman TW, Binder HJ: Serotonin-induced alteration of colonic electrolyte transport in the rat. Gastroenterology 86:310–317, 1984

    Google Scholar 

  67. Hardcastle J, Hardcastle PT, Redfern JS: Action of 5-hydroxytryptamine on intestinal transport in the rat. J Physiol 320:41–55, 1981

    Google Scholar 

  68. Donowitz M, Tai YH, Asarkof N: Effect of serotonin on active electrolyte transport in rabbit ileum, gallbladder and colon. Am J Physiol 239:G463–472, 1980

    Google Scholar 

  69. Gaginella TS, Rimele TJ, Wietecha M: Studies on rat intestinal cell receptors for serotonin and opiates. J Physiol 335:101–111, 1983

    Google Scholar 

  70. Branghek T, Kates M, Gershon MD: Enteric receptors for 5-hydroxytryptamine. Brain Res 324:107–118 1984

    Google Scholar 

  71. Munck LK, Mertz-Nielsen A, Westh H, Bukhave K, Beubler E, Rask-Madsen J: Prostaglandin E2 is a mediator of 5-hydroxytryptamine induced water and electrolyte secretion in the human jejunum. Gut 29:1337–1341, 1988

    Google Scholar 

  72. Beubler E, Horina G: 5-HT2 and 5-HT3 receptor subtypes mediate cholera toxin-induced intestinal fluid secretions in the rat. Gastroenterology 99:83–89, 1990

    Google Scholar 

  73. Yau WM, Dorsett JA, Youther ML: Modulation of submucosal cholinergic neurones by 5-hydroxytryptamine and neuropeptides. Am J Physiol 259:G1019–1024, 1990

    Google Scholar 

  74. Donowitz M, Binder HJ: Jejunal fluid and electrolyte secretion in carcinoid syndrome. J Dig Dis 20:1115–1122, 1975

    Google Scholar 

  75. Cassuto J, Jodal M, Tuttle R, Lundgren O: 5-Hydroxytryptamine and cholera secretion. Scand J Gastroenterol 17:695–703, 1982

    Google Scholar 

  76. Jackson JC, Cross RJ, Walker RF, Markesbert WR, Brooks WH, Roszman TL: Influence of serotonin on the immune response. Immunology 54:505–512, 1985

    Google Scholar 

  77. Marquardt DL, Gruber HE, Wassermann SI: Adenosine release from stimulated mast cells. Proc Natl Acad Sci USA 81:6192–6196, 1984

    Google Scholar 

  78. Stiles GL: Adenosine receptors: Physiological regulation and biochemical mechanisms. News Physiol Sci 6:161–165, 1991

    Google Scholar 

  79. Dobbins JW, Laurenson JP, Forrest JN Jr: Adenosine and adenosine analogues stimulate adenosine cyclic 3′, 5′-monophosphate-dependent chloride secretion in the mammalian intestine. J Clin Invest 74:929–935, 1984

    Google Scholar 

  80. Barrett KE, Cohn JA, Huott PA, Wassermann S, Dharmsathaphorn K: Immune-related intestinal secretion. Effect of adenosine on T84 cell line. Am J Physiol 258:C902-C912, 1990

    Google Scholar 

  81. Barrett KE, Huott PA, Shah SS, Dharmsathaphorn K, Wassermann SI: Differing effects of apical and basolateral adenosine on colonic epithelial cell line T84. Am J Physiol 256:C197-C203, 1989

    Google Scholar 

  82. Dho S, Stewart K, Foskett JK: Purinergic receptor activation of Cl secretion in T84 cells. Am J Physiol 262:C67-C74, 1992

    Google Scholar 

  83. Doring A, Diener M, Rummel W: Arachidonic acid-induced secretion in the rat colon: Indomethacin-resistant neuronal and epithelial actions. Eicosanoids 3:149–154, 1990

    Google Scholar 

  84. Smith WL, Borgeat P: Theeicosanoids: Prostaglandins, thromboxanes, leukotrienes, and hydroxy-eicosaenic acids.In Biochemistry of Lipids and Membranes. DE Vance, JE Vance (eds). Amsterdam, Benjamin/Cummings Publishing, 1985, pp 325–360

    Google Scholar 

  85. Czop JK, Austen KF: Generation of leukotrienes by human monocytes upon stimulation of their β-glycan receptor during phagocytosis. Proc Natl Acad Sci USA 82:2751–2755, 1985

    Google Scholar 

  86. Craven PA, DeRubertis FR: Profiles of eicosanoid production by superficial and proliferative colonic epithelial cells and sub-epithelial colonic tissue. Prostaglandins 32:387–399, 1986

    Google Scholar 

  87. Smith PL: Effects of the neuroimmune mediators, peptioleukotrienes, endothelin, and interleukin-1 on intestinal ion transport. Ann NY Acad Sci 664:260–274, 1992

    Google Scholar 

  88. Smith PL, Montzka DP, McCafferty GP, Wasserman MA, Fondacaro JD: Effect of sulfidopeptide leukotrienes D4 and E4 on ileal ion transport in the rat and rabbit. Am J Physiol 255:G175-G183, 1988

    Google Scholar 

  89. Smith PL, Chissone DC, McCafferty GP: Characterisation of LTC4 effects on rabbit ileal mucosa. Naunyn-Schmiedeberg's Arch Pharmacol 341:94–100, 1990

    Google Scholar 

  90. Lawson LD, Powell DW: Bradykinin-stimulated eicosanoid synthesis and secretion of rabbit ileal components. Am J Physiol 252:G783-G790, 1987

    Google Scholar 

  91. Crane PA, DeRubertis FR: Patterns of prostaglandin synthesis and degradation in isolated superficial and proliferative colonic epithelial cells compared to residual colon. Prostaglandins 225:583–604, 1983

    Google Scholar 

  92. Gaginella TS: Eicosanoid-mediated intestinal secretion.In Textbook of Secretory Diarrhea. E Lebenthal, M Duffy (eds). New York, Raven Press, 1990, pp 15–30

    Google Scholar 

  93. Musch MW, Field M, Miller RJ, Staff JS: Homologous desensitisation of prostaglandins in rabbit ileum. Am J Physiol 252:G120-G127, 1987

    Google Scholar 

  94. Racusen LC, Binder HJ: Effect of prostaglandins on ion transport across isolated colonic epithelium. Dig Dis Sci 25:900–904, 1980

    Google Scholar 

  95. Wu-Wang C-Y, Wang SL, Stevens B, Neu J: Localisation and characterization of prostaglandin E1 receptors in the rat small intestine. Prostaglandins Leukotrienes Essent Fatty Acids 36:129–134, 1989

    Google Scholar 

  96. Halm DR, Rechkemmer GR, Schoumacher RA, Frizzell RA: Apical membrane chloride channels in colonic cells line activated by secretory agonists. Am J Physiol 254:C505-C511, 1988

    Google Scholar 

  97. Rangachari PK: Concerning prostaglandin D2: Forgotten, promiscuous, capricious. Ann NY Acad Sci 664:248–259, 1992

    Google Scholar 

  98. Bjarnason I, Smethurst P, Clark P, Menzies J, Levi J, Peters T: Effects of prostaglandin on indomethacins-induced increased intestinal permeability in man. Scand J Gastroenterol 24(suppl 164):97–103, 1989

    Google Scholar 

  99. Ma TY, Hollander D, Erickson RA, Truong H, Krugliak P: Is the small intestinal epithelium truly tight to inulin permeability. Am J Physiol 260:G669-G679, 1991

    Google Scholar 

  100. Phipps RP, Stein SH, Roper RL: A new view on prostaglandin E regulation of the immune response. Immunol Today 12:349–352, 1991

    Google Scholar 

  101. Uribe A, Johansson C: Initial kinetic changes of prostaglandin E2-induced hyperplasia of the rat small intestinal epithelium occur in the villus compartments. Gastroenterology 94:1325–1342, 1988

    Google Scholar 

  102. Craven PA, Saito R, DeRubertis FR: Role of local prostaglandin synthesis in the modulation of proliferative activity of rat colonic epithelium. J Clin Invest 72:1365–1375, 1983

    Google Scholar 

  103. O'Flaherty JP: Neutrophil degranulation: Evidence pertaining to its mediation by the combined effects of leukotriene B4, platelet-activating factor and 5-HETE. J Cell Physiol 122:229–239, 1985

    Google Scholar 

  104. Bern MJ, Sturbaum CW, Karayalcin SS, Bershneider HJ, Washman JT, Powell DW: Immune control of rat and rabbit colonic electrolyte transport: Role of prostaglandins and enteric nervous system. J Clin Invest 83:1810–1820, 1989

    Google Scholar 

  105. Hanglow AC, Bienenstock J, Perdue MH: Effects of platelet-activating factor on ion transport in isolated rat jejunum. Am J Physiol 257:G845-G850, 1989

    Google Scholar 

  106. Parks DA: Oxygen radicals: Mediators of gastrointestinal pathophysiology. Gut 30:293–298, 1989

    Google Scholar 

  107. Klebanoff SJ: Phagocytic cells: Products of oxygen metabolism.In Inflammation: Basic Principles and Clinical Correlates. JI Gallin, IM Goldstein (eds). New York, Raven Press, 1988, pp 391–449

    Google Scholar 

  108. Karayalcin SS, Sturbaum CW, Wachsman JT, Cha J-H, Powell DW: Hydrogen peroxide stimulates rat colonic prostaglandin production and alters electrolyte transport J Clin Invest 86:60–68, 1990

    Google Scholar 

  109. Shasby DM, Winter M, Shasby SS: Oxidants and conductance of cultured epithelial cell monolayers: Inositol phospholipid hydrolysis. Am J Physiol 225:C781-C788, 1988

    Google Scholar 

  110. Murthy SNS, Cooney CG, Clearfield NR: Hydrogen peroxide-induced alterations in prostaglandin secretion in the rat colonin vitro. Inflammation 14:645–661, 1990

    Google Scholar 

  111. Tamai H, Gaginella TS, Kachur JF, Musch MW, Chang EB: Ca-mediated stimulation of Cl secretion by reactive oxygen metabolites in human colonic T84 cells. J Clin Invest 89301–307, 1992

    Google Scholar 

  112. Grisham MB, Gaginella TS, von Ritter C, Tamai H, Be RM, Granger DN: Effects of neutrophil-derived oxidants on intestinal permeability, electrolyte transport and epithelial cell viability. Inflammation 14:531–542, 1990

    Google Scholar 

  113. Grisham MB, von Ritter C, Smith BF, LaMont JT, Granger DN: Interaction between oxygen radicals and gastric mucin. Am J Physiol 253:G93-G96, 1987

    Google Scholar 

  114. Lamont JT: Mucus: The front line of mucosal defence. Ann NY Acad Sci 664:190–201, 1992

    Google Scholar 

  115. Gregory SH, Magee DM, Wing EJ: The role of colonystimulating factors in host defences. Proc Soc Exp Biol Med 197:349–360, 1991

    Google Scholar 

  116. Kelso A: Cytokines: Structure, function and synthesis. Curr Opin Immunol 2:215–225, 1989

    Google Scholar 

  117. Cominelli F: Cytokines in the gastrointestinal tract.In Immunopharmacology of the Gastrointestinal System. JL Wallace (ed). London, Academic Press, 1993, pp 123–136

    Google Scholar 

  118. Chissone DC, Simon PL, Smith PL: Interleukin-1: Effects on rabbit ileal mucosal ion transportin vitro. Eur J Pharmacol 189:217–228, 1990

    Google Scholar 

  119. Cominelli F, Nast CC, Dinarello CA, Gentilini P, Zipser RD: Regulation of eicosanoid production in rabbit colon by interleukin-1. Gastroenterology 97:1400–1405, 1989

    Google Scholar 

  120. Chang EB, Musch MW, Mayer L: Interleukins 1 and 3 stimulate anion secretion in chicken intestine. Gastroenterology 98:1518–1524, 1990

    Google Scholar 

  121. Dinarello GA: Interleukin-1 and its biologically related cytokines. Adv Immunol 44:153–205, 1989

    Google Scholar 

  122. Rosenberg SA, Lotze MT, Mule JJ: New approaches to immunotherapy of cancer using interleukin 2. Ann Intern Med 108:853–864, 1988

    Google Scholar 

  123. Coffman RL, Seymour BWP, Hudak S, Jackson J, Rennick D: Antibody to interleukin-5 inhibits helminth induced eosinophilia in mice. Science 245:308–310, 1989

    Google Scholar 

  124. Humbert JR, Winsor El: Tumor necrosis factor primes neutrophils by shortening the lag period of the respiratory burst. Am J Med Sci 300:209–213, 1990

    Google Scholar 

  125. Kandil H, Berschneider H, Argenzio A: TNFα alters intestinal ion transport through a paracrine mechanism involving prostaglandins. Gastroenterology 102:A217, 1992 (abstract)

    Google Scholar 

  126. Mullin JM, Snock KV: Effect of tumour necrosis factor on the epithelial tight junction and transepithelial permeability. Cancer Res 50:2172–2176, 1990

    Google Scholar 

  127. Holmgren J, Frylund J, Larsson H: Gamma-interferonmediated down-regulation of electrolyte secretion by intestinal epithelial cell: A local immune mechanism? Scand J Immunol 30:499–503, 1989

    Google Scholar 

  128. Madara J, Stafford J: Interferon-γ affects barrier function of cultured intestinal epithelial monolayers. J Clin Invest 83:724–727, 1989

    Google Scholar 

  129. Coleman JW, Buckley MG, Holliday MR, Morris AG: Interferon-γ inhibits serotonin release from mouse peritoneal mast cells. Eur J Immunol 21:2559–2564, 1991

    Google Scholar 

  130. Swieter M, Ghali WA, Rimmer C, Befus D: Interferon α/β inhibits IgE-dependent histamine release from rat mast cells. Immunology 66:606–610, 1989

    Google Scholar 

  131. Boraschi D, Censini S, Bartalini M, Scapigliati G, Barbarulli G, Vicenzi E, Donati MB, Tagliabue A: Interferon inhibits prostaglandin synthesis in macrophages: Effect on arachidonic metabolism. J Immunol 132:1987–1992, 1984

    Google Scholar 

  132. McKay DM, Perdue MH: Interferon α/β reduces antigen-induced jejunal secretion in the rat. Gastroenterology 102:A225, 1992 (abstract)

    Google Scholar 

  133. Pfeffer LM, Landsberger FR, Tamm I: Beta-interferon-induced time-dependent changes in plasma membrane lipid bilayer of cultured cell. J Interferon Res 4:613–620, 1981

    Google Scholar 

  134. Koyama S-Y, Podolsky DK: Differential expression of transforming growth factors α and β in rat intestinal epithelial cells. J Clin Invest 83:1768–1773, 1989

    Google Scholar 

  135. Barnard JA, Polk WH, Moses HL, Coffey RJ: Production of transforming growth factor-α by normal rat small intestine. Am J Physiol 261:C994-C1000, 1991

    Google Scholar 

  136. Madsen-Opleta K, Hardin J, Gall DG: Epidermal growth factor upregulates intestinal electrolyte and nutrient transport Am J Physiol 260:G807-G814, 1991

    Google Scholar 

  137. Niessen HWM, Kuijpers TW, Ross D, Verhoeven AJ: Release of azurophilic granule contents in fMLP stimulated neutrophils requires two activation signals, one of which is a rise in cytosolic free Ca2+. Cell. Signal 3:625–633, 1991

    Google Scholar 

  138. von Ritter C, Grisham MB, Hollwarth M, Inauen W, Granger ND: Neutrophil-derived oxidants mediate formylmethionyl-leucyl-phenylalanine-induced increases in mucosal permeability in rats. Gastroenterology 97:778–780, 1989

    Google Scholar 

  139. Nash S, Stafford J, Madara JL: The selective and superoxide-independent disruption of intestinal epithelial tight junctions during leucocyte transmigration. Lab Invest 59:531–537, 1988

    Google Scholar 

  140. Bland PW, Warren LG: Antigen presentation by epithelial cell of the rat intestine. II Selective induction of suppressor T cell. Immunology 58:9–14, 1986

    Google Scholar 

  141. Kaiserlain D: Murine gut epithelial cells express Ia molecules antigenically distinct from the conventional antigenpresenting cells. Immunol Res 10:360–364, 1991

    Google Scholar 

  142. Masson SD, Perdue MH: Changes in distribution of Ia antigen on epithelium of the jejunum and ileum in rats infected withNippostrongylus brasiliensis. Clin Immunol Immunopathol 57:83–95, 1990

    Google Scholar 

  143. Targan SR, Deem RL, Shanahan F: Role of mucosal T-cell-generated cytokines in epithelial cell injury. Immunol Res 10:472–478, 1991

    Google Scholar 

  144. Mayer L, Shlien R: Evidence for function of Ia molecules on gut epithelial cells in man. J Exp Med 166:1471–1483, 1987

    Google Scholar 

  145. Bland PW, Kambarage DM: Antigen handling by the epithelium and lamina propria macrophages. Gastroenterol Clin North Am 20:577–596, 1990

    Google Scholar 

  146. Shirota K, LeDuy L, Yuan S, Jothy S: Interleukin-6 and its receptor are expressed in human intestinal epithelial cells. Virchows Arch B Cell Pathol 58:303–308, 1990

    Google Scholar 

  147. Shanahan WR Jr, Hancock WW, Korn JH: Expression of IL-1 and tumour necrosis, factor by epithelial cells: Role in stimulating fibroblast PGE2 synthesis. J Exp Pathol 4:17–27, 1988

    Google Scholar 

  148. Perdue MH, Marshall J, Masson S: Ion transport abnormalities in inflamed rat jejunum. Gastroenterology 98:562–567, 1990

    Google Scholar 

  149. Perdue MH, Ramage JK, Burget D, Marshall J, Masson S: Intestinal mucosal injury is associated with mast cell activation and leukotriene generation duringNippostrongylus-induced inflammation in the rat. Dig Dis Sci 34:724–731, 1989

    Google Scholar 

  150. D'Inca R, Ramage JK, Hunt RH, Perdue MH: Antigen-induced mucosal damage and restitution in the small intestine of the immunized rat. Int Arch Allergy Appl Immunol 91:270–277, 1990

    Google Scholar 

  151. Ramage JK, Stanisz A, Scicchitano R, Hunt RH, Perdue MH: Effect of immunologic reactions on rat intestinal permeability. Correlation of increased permeability to chromium 51-labelled ethylenediaminetetraacetic acid and ovalbumin during acute inflammation and anaphylaxis. Gastroenterology 94:1368–1375, 1988

    Google Scholar 

  152. Zhang S, Myers S, Castro GA: Inhibition of anaphylaxisevoked intestinal fluid secretion by the dual application of an H1-antagonist and cyclooxygenase inhibitor. Gastroenterology 100:922–928, 1991

    Google Scholar 

  153. Castro GA, Harari Y, Russell D: Mediators of anaphylaxis-induced ion transport changes in small intestine. Am J Physiol 253:G540–548, 1987

    Google Scholar 

  154. Castro GA, Harari Y: Intestinal epithelial membrane changes in rats immune toTrichinella spiralis. Mol Biochem Parasitol 6:191–204, 1982

    Google Scholar 

  155. Castro GA, Hessel JJ, Whalen G: Altered intestinal fluid movement in response toTrichinella spiralis in immunised rats. Parasite Immunol 1:259–266, 1979

    Google Scholar 

  156. Castro GA, Roy SA, Stockstill RD:Trichinella spiralis: Peroxidase activity in isolated cells from the rat intestine. Exp Parasitol 36:307–315, 1974

    Google Scholar 

  157. Crowe SE, Sestini P, Perdue MH: Allergic reactions of rat jejunal mucosa. Ion transport responses to luminal antigen and inflammatory mediators. Gastroenterology 99:74–82, 1990

    Google Scholar 

  158. Crowe SE, Soda K, Stanisz AM, Perdue MH: Intestinal permeability in allergic rats: Abnormalities before and after antigen challenge. Am J Physiol 1993 (in press)

  159. Perdue MH, Masson S, Wershill BK, Galli SJ: Role of mast cells in ion transport abnormalities associated with intestinal anaphylaxis. Correction of diminished secretory response in genetically mast cell-deficientW/W v mice by bone-marrow transplantation. J Clin Invest 87:688–693, 1991

    Google Scholar 

  160. Curtis GH, Patrick MK, Catto-Smith AG, Gall DG: Intestinal anaphylaxis in the rat: Effect of chronic antigen exposure. Gastroenterology 98:1558–1566, 1990

    Google Scholar 

  161. Baron DA, Baird AW, Cuthbert AW, Margoluis HS: Intestinal anaphylaxis: Rapid changes in mucosal ion transport and morphology. Am J Physiol 254:G307-G314, 1988

    Google Scholar 

  162. Baird AW, Coombs RRA, McLaughlin P, Cuthbert AW: Immediate hypersensitivity reactions to cow milk proteins in isolated epitheliums from ileum of milk drinking guinea pigs: Comparison with colonic epithelia. Int Arch Allergy Appl Immunol 75:255–263, 1984

    Google Scholar 

  163. Rousset M: The human colon carcinoma cell lines HT-29 and CaCo-2: Twoin vitro models for study of intestinal differentiation. Biochemie 68:1035–1040, 1986

    Google Scholar 

  164. Hidalgo IJ, Raub TJ, Borchardt: Characterisation of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelia permeability. Gastroenterology 96:736–749, 1989

    Google Scholar 

  165. Vaandrager AB, Bajnath R, Groot JA, Bot AGM, de Jonge HR: Ca2+ and cAMP activate different chloride efflux pathways in HT-29.c119A colonic epithelia cell line. Am J Physiol 261:G958-G965, 1991

    Google Scholar 

  166. Gustafson C, Lindahl M, Tagesson C: Hydrogen peroxide stimulates phospholipase A2-mediated arachidonic acid release in cultured intestinal epithelial cells (INT 407). Scand J Gastroenterol 26:237–247, 1991

    Google Scholar 

  167. Baird AW, Cuthbert AW, MacVinish LJ: Type 1 hypersensitivity reactions in reconstructed tissues using syngeneic cell types. Br J Pharmacol 91:857–869, 1987

    Google Scholar 

  168. Crowe SE, Perdue MH: Gastrointestinal food hypersensitivity: Basic mechanisms of pathophysiology. Gastroenterology 103:1075–1095, 1992

    Google Scholar 

  169. van Rosendall GMA: Recent advances in pharmacotherapy: Inflammatory bowel disease. Can Med Assoc J 141:113–124, 1989

    Google Scholar 

  170. Hodgson HJF, Jewell DP: Immunology of inflammatory bowel disease. Bailliere's Clin Gastroenterol 1:531–545, 1987

    Google Scholar 

  171. Ericsson CD, Evans DG, DuPont HL, Evand DJ Jr, Pickering LK: Bismuth subsalicylate inhibits activity of crude toxins ofEscherichia coli andVibrio cholerae. J Infect Dis 136:693–696, 1977

    Google Scholar 

  172. Wallace JL, Keenan CM, Granger DN: Gastric ulceration induced by nonsteroidal anti-inflammatory drugs is a neutrophil-dependent process. Am J Physiol 259:G462-G467, 1990

    Google Scholar 

  173. Rampton DS, Hawley CJ: Prostaglandins and ulcerative colitis. Gut 25:1399–1413, 1984

    Google Scholar 

  174. Benton HP: Cytokines and their receptors. Curr Opin Cell Biol 3:171–175, 1991

    Google Scholar 

  175. Fernandez-Botran R: Soluble cytokine receptors: Their role in immunoregulation. FASEB J 5:2567–2574, 1991

    Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

McKay, D.M., Perdue, M.H. Intestinal epithelial function: The case for immunophysiological regulation. Digest Dis Sci 38, 1735–1745 (1993). https://doi.org/10.1007/BF01303185

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01303185

Key Words

  • immunophysiology
  • intestinal hypersensitivity
  • immune system
  • mast cell
  • inflammatory mediator
  • cytokine
  • ion secretion
  • anaphylaxis
  • secretory disease