Skip to main content
NCBI home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1992 Jan;89(1):301–307. doi: 10.1172/JCI115576

Ca-mediated stimulation of Cl secretion by reactive oxygen metabolites in human colonic T84 cells.

H Tamai 1, T S Gaginella 1, J F Kachur 1, M W Musch 1, E B Chang 1
PMCID: PMC442848  PMID: 1729277

Abstract

Monochloramine (NH2Cl), a granulocyte-derived reactive oxygen metabolite (ROM), increases short-circuit current (Isc) in cultured T84 monolayers in a concentration-dependent manner up to nonlethal concentrations of 75 microM. Isc increases slowly after NH2Cl, reaching a peak value of 18 +/- 2 microA/cm2 20 min after addition. The Isc changes are persistent (lasting over 20-30 min), depend on medium Cl, and are inhibitable with bumetanide. 36Cl flux studies demonstrated that NH2Cl increases serosa-to-mucosa flux of Cl without changing mucosa-to-serosa flux, consistent with stimulation of electrogenic Cl secretion. Isc responses to NH2Cl, but not PGE2, are dependent on medium calcium. As demonstrated in fura-2-loaded T84 cells, NH2Cl increases free cytosolic calcium by influx of extracellular Ca2+ and by release of Ca2+ from endogenous stores. However, NH2Cl had no effect on phosphatidylinositol metabolism or cyclic nucleotide levels. We conclude that ROM directly stimulate electrolyte secretion, an effect in part mediated by increases in cytosolic Ca2+, possibly through increasing Ca2+ permeability of cellular membranes.

Full text

PDF
301

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barrett K. E., Cohn J. A., Huott P. A., Wasserman S. I., Dharmsathaphorn K. Immune-related intestinal chloride secretion. II. Effect of adenosine on T84 cell line. Am J Physiol. 1990 May;258(5 Pt 1):C902–C912. doi: 10.1152/ajpcell.1990.258.5.C902. [DOI] [PubMed] [Google Scholar]
  2. Bellomo G., Mirabelli F., Richelmi P., Orrenius S. Critical role of sulfhydryl group(s) in ATP-dependent Ca2+ sequestration by the plasma membrane fraction from rat liver. FEBS Lett. 1983 Oct 31;163(1):136–139. doi: 10.1016/0014-5793(83)81180-6. [DOI] [PubMed] [Google Scholar]
  3. Bern M. J., Sturbaum C. W., Karayalcin S. S., Berschneider H. M., Wachsman J. T., Powell D. W. Immune system control of rat and rabbit colonic electrolyte transport. Role of prostaglandins and enteric nervous system. J Clin Invest. 1989 Jun;83(6):1810–1820. doi: 10.1172/JCI114086. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  5. CABAUD P. G., WROBLEWSKI F. Colorimetric measurement of lactic dehydrogenase activity of body fluids. Am J Clin Pathol. 1958 Sep;30(3):234–236. doi: 10.1093/ajcp/30.3.234. [DOI] [PubMed] [Google Scholar]
  6. Cartwright C. A., McRoberts J. A., Mandel K. G., Dharmsathaphorn K. Synergistic action of cyclic adenosine monophosphate- and calcium-mediated chloride secretion in a colonic epithelial cell line. J Clin Invest. 1985 Nov;76(5):1837–1842. doi: 10.1172/JCI112176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chang E. B., Musch M. W. Calcium mediated neurohumoral inhibition of chicken enterocyte Na influx: role of phosphatidylinositol metabolites. Life Sci. 1990;46(26):1913–1921. doi: 10.1016/0024-3205(90)90506-m. [DOI] [PubMed] [Google Scholar]
  8. Grinstein S., Rothstein A., Sarkadi B., Gelfand E. W. Responses of lymphocytes to anisotonic media: volume-regulating behavior. Am J Physiol. 1984 Mar;246(3 Pt 1):C204–C215. doi: 10.1152/ajpcell.1984.246.3.C204. [DOI] [PubMed] [Google Scholar]
  9. Grisham M. B., Gaginella T. S., von Ritter C., Tamai H., Be R. M., Granger D. N. Effects of neutrophil-derived oxidants on intestinal permeability, electrolyte transport, and epithelial cell viability. Inflammation. 1990 Oct;14(5):531–542. doi: 10.1007/BF00914274. [DOI] [PubMed] [Google Scholar]
  10. Huott P. A., Liu W., McRoberts J. A., Giannella R. A., Dharmsathaphorn K. Mechanism of action of Escherichia coli heat stable enterotoxin in a human colonic cell line. J Clin Invest. 1988 Aug;82(2):514–523. doi: 10.1172/JCI113626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kako K., Kato M., Matsuoka T., Mustapha A. Depression of membrane-bound Na+-K+-ATPase activity induced by free radicals and by ischemia of kidney. Am J Physiol. 1988 Feb;254(2 Pt 1):C330–C337. doi: 10.1152/ajpcell.1988.254.2.C330. [DOI] [PubMed] [Google Scholar]
  12. Kaneko M., Beamish R. E., Dhalla N. S. Depression of heart sarcolemmal Ca2+-pump activity by oxygen free radicals. Am J Physiol. 1989 Feb;256(2 Pt 2):H368–H374. doi: 10.1152/ajpheart.1989.256.2.H368. [DOI] [PubMed] [Google Scholar]
  13. Karayalcin S. S., Sturbaum C. W., Wachsman J. T., Cha J. H., Powell D. W. Hydrogen peroxide stimulates rat colonic prostaglandin production and alters electrolyte transport. J Clin Invest. 1990 Jul;86(1):60–68. doi: 10.1172/JCI114715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Mandel K. G., McRoberts J. A., Beuerlein G., Foster E. S., Dharmsathaphorn K. Ba2+ inhibition of VIP- and A23187-stimulated Cl- secretion by T84 cell monolayers. Am J Physiol. 1986 Mar;250(3 Pt 1):C486–C494. doi: 10.1152/ajpcell.1986.250.3.C486. [DOI] [PubMed] [Google Scholar]
  15. Murphy S. N., Miller R. J. Regulation of Ca++ influx into striatal neurons by kainic acid. J Pharmacol Exp Ther. 1989 Apr;249(1):184–193. [PubMed] [Google Scholar]
  16. Musch M. W., Nahkla A. M., Chang E. B. Phorbol ester-stimulated secretion in chicken ileum: role of arachidonic acid metabolism. Gastroenterology. 1990 Aug;99(2):393–400. doi: 10.1016/0016-5085(90)91021-w. [DOI] [PubMed] [Google Scholar]
  17. Okabe E., Hess M. L., Oyama M., Ito H. Characterization of free radical-mediated damage of canine cardiac sarcoplasmic reticulum. Arch Biochem Biophys. 1983 Aug;225(1):164–177. doi: 10.1016/0003-9861(83)90020-6. [DOI] [PubMed] [Google Scholar]
  18. Reinlib L., Mikkelsen R., Zahniser D., Dharmsathaphorn K., Donowitz M. Carbachol-induced cytosolic free Ca2+ increases in T84 colonic cells seen by microfluorimetry. Am J Physiol. 1989 Dec;257(6 Pt 1):G950–G960. doi: 10.1152/ajpgi.1989.257.6.G950. [DOI] [PubMed] [Google Scholar]
  19. Tamai H., Kachur J. F., Baron D. A., Grisham M. B., Gaginella T. S. Monochloramine, a neutrophil-derived oxidant, stimulates rat colonic secretion. J Pharmacol Exp Ther. 1991 May;257(2):887–894. [PubMed] [Google Scholar]
  20. Tamai H., Kachur J. F., Grisham M. B., Gaginella T. S. Scavenging effect of 5-aminosalicylic acid on neutrophil-derived oxidants. Possible contribution to the mechanism of action in inflammatory bowel disease. 1991 Mar 15-Apr 1Biochem Pharmacol. 41(6-7):1001–1006. doi: 10.1016/0006-2952(91)90207-l. [DOI] [PubMed] [Google Scholar]
  21. Thomas E. L., Grisham M. B., Jefferson M. M. Preparation and characterization of chloramines. Methods Enzymol. 1986;132:569–585. doi: 10.1016/s0076-6879(86)32042-1. [DOI] [PubMed] [Google Scholar]
  22. Volpe P., Krause K. H., Hashimoto S., Zorzato F., Pozzan T., Meldolesi J., Lew D. P. "Calciosome," a cytoplasmic organelle: the inositol 1,4,5-trisphosphate-sensitive Ca2+ store of nonmuscle cells? Proc Natl Acad Sci U S A. 1988 Feb;85(4):1091–1095. doi: 10.1073/pnas.85.4.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Warhurst G., Higgs N. B., Lees M., Tonge A., Turnberg L. A. Activation of protein kinase C attenuates prostaglandin E2 responses in a colonic cell line. Am J Physiol. 1988 Jul;255(1 Pt 1):G27–G32. doi: 10.1152/ajpgi.1988.255.1.G27. [DOI] [PubMed] [Google Scholar]
  24. Wasserman S. I., Barrett K. E., Huott P. A., Beuerlein G., Kagnoff M. F., Dharmsathaphorn K. Immune-related intestinal Cl- secretion. I. Effect of histamine on the T84 cell line. Am J Physiol. 1988 Jan;254(1 Pt 1):C53–C62. doi: 10.1152/ajpcell.1988.254.1.C53. [DOI] [PubMed] [Google Scholar]
  25. Watanabe H., Kobayashi A., Yamamoto T., Suzuki S., Hayashi H., Yamazaki N. Alterations of human erythrocyte membrane fluidity by oxygen-derived free radicals and calcium. Free Radic Biol Med. 1990;8(6):507–514. doi: 10.1016/0891-5849(90)90150-h. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES