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Longitudinal smooth muscle of the mammalian intestine

A model for Ca2+ signaling by cADPR

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Abstract

Ca2+ mobilization in muscle cells from the circular muscle layer of the mammalian intestine is mediated by IP3-dependent Ca2+ release. Ca2+ mobilization in muscle from the adjacent longitudinal muscle layer involves a distinct, phosphoinositide-independent pathway. Receptors for contractile agonists in longitudinal muscle cells are coupled via a pertussis toxinsensitive G protein to activation of PLA2 and formation of arachidonic acid (AA). The latter activates Cl− channels resulting in depolarization of the plasma membrane and opening of voltage-sensitive Ca2+ channels. Ca2+ influx via these channels induces Ca2+ release by activating sarcoplasmic ryanodine receptor/Ca2+ channels. The increase in [Ca2+]i activates membrane-bound ADP ribosyl cyclase, and the resultant formation of cADPR enhances Ca2+-induced Ca2+ release.

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Abbreviations

cADPR:

cyclic adenosine diphospho-ribose

ADP ribosyl cyclase:

adenosine diphospho-ribosyl cyclase

β-NAD+ :

β-nicotinamide adenine dinucleotide, reduced form

IP3 :

inositol 1,4,5-trisphosphate

PIP2 :

phosphatidylinositol 4,5-bis-phosphate

PIP:

phosphatidylinositol 4-monophosphate

PLA2 :

phospholipase A2

AA:

arachidonic acid

CCK-8:

cholecystokinin octapeptide

GDPβS:

guanosine 5′-0-(β-thio) diphosphate

References

  1. Grider, J. R. and Makhlouf, G. M. (1988) Contraction mediated by Ca2+ release in circular and Ca2+ influx in longitudinal intestinal muscle cells.J. Pharmacol. Exp. Ther. 244, 432–437.

    PubMed  CAS  Google Scholar 

  2. Bitar, K. N., Bradford, P. G., Putney, J. W., Jr., and Makhlouf, G. M. (1986) Cytosolic calcium during contraction of isolated mammalian gastric muscle cells.Science 232, 1143–1145.

    Article  PubMed  CAS  Google Scholar 

  3. Bitar, K. N., Bradford, P. G., Putney, J. W., Jr., and Makhlouf, G. M. (1986) Stoichiometry of contraction and Ca2+ mobilization by inositol 1,4,5-trisphosphate in isolated gastric smooth muscle cells.J. Biol. Chem. 261, 16,591–16,596.

    CAS  Google Scholar 

  4. Murthy, K. S., Grider, J. R., and Makhlouf, G. M. (1991) InsP3-dependent Ca2+ mobilization in circular but not longitudinal muscle cells of intestine.Am. J. Physiol. 261, G937-G944.

    PubMed  CAS  Google Scholar 

  5. Murthy, K. S. and Makhlouf, G. M. (1991) Phosphoinositide metabolism in intestinal smooth muscle: preferential production of Ins(1,4,5)P3 in circular muscle cells.Am. J. Physiol. 261, G945-G951.

    PubMed  CAS  Google Scholar 

  6. Kuemmerle, J. F., Murthy, K. S., and Makhlouf, G. M. (1994) Agonist-activated, ryanodine-sensitive, IP3-insensitive Ca2+ release channels in longitudinal muscle of intestine.Am. J. Physiol. 266, C1421-C1431.

    PubMed  CAS  Google Scholar 

  7. Murthy, K. S., Kuemmerle, J. F., and Makhlouf, G. M. (1995) Agonist-mediated activation of PLA2 initiates Ca2+ mobilization in intestinal longitudinal muscle.Am. J. Physiol. 269, G93-G102.

    PubMed  CAS  Google Scholar 

  8. Wang, X-B., Osugi, T., and Uchida, S. (1992) Different pathways for Ca2+ influx and intracellular release of Ca2+ mediated by muscarinic receptors in ileal longitudinal smooth muscle.Jpn. J. Pharmacol. 58, 407–415.

    Article  PubMed  CAS  Google Scholar 

  9. Wang, X-B., Osugi, T., and Uchida, S. (1993) Muscarinic receptors stimulate Ca2+ influx via phospholipase A2 pathway in ileal smooth muscle.Biochem. Biophys. Res. Comm. 193, 483–489.

    Article  PubMed  CAS  Google Scholar 

  10. Anderson, M. P. and Welsh, M. J. (1990) Fatty acids inhibit apical membrane chloride channels in airway epithelia.Proc. Natl. Acad. Sci. USA 87, 7334–7338.

    Article  PubMed  CAS  Google Scholar 

  11. Ordway, R. W., Walsh, J. V., Jr., and Singer, J. J. (1989) Arachidonic acid and other fatty acids directly activate potassium channels in smooth muscle cells.Science 244, 1176–1179.

    Article  PubMed  CAS  Google Scholar 

  12. Shimada, T. and Somlyo, A. P. (1992) Modulation of voltage dependent Ca channels current by arachidonic acid and other long-chain fatty acid in intestinal muscle.J. Gen. Physiol. 100, 27–44.

    Article  PubMed  CAS  Google Scholar 

  13. Inoue, R. and Isenberg, G. (1990) Acetylcholine activates nonselective cation channels in guinea pig ileum through a G protein.Am. J. Physiol. 258, C1173-C1178.

    PubMed  CAS  Google Scholar 

  14. Sun, X-P., Supplisson, S., and Mayer, E. (1993) Chloride channels in myocytes from rabbit colon are regulated by a pertussis toxinsensitive G protein.Am. J. Physiol. 264, G774-G785.

    PubMed  CAS  Google Scholar 

  15. Kuemmerle, J. F. and Makhlouf, G. M. (1994) Activation of Cl− channels by contractile agonists depolarizes longitudinal muscle and triggers Ca2+ influx via voltage-sensitive Ca2+ channels.Gastroenterology 106, A527.

    Google Scholar 

  16. Kuemmerle, J. F. and Makhlouf, G. M. (1995) Agonist-stimulated cyclic ADP ribose: endogenous modulation of Ca2+-induced Ca2+ release in intestinal longitudinal muscle.J. Biol. Chem. 270, 25,488–25,494.

    CAS  Google Scholar 

  17. Anderson, K., Lai, F. A., Liu, Q., Rousseau, E., Erickson, H. P., and Meissner, G. (1989) Structural and functional characterization of the purified cardiac ryanodine receptor Ca2+ release channel complex.J. Biol. Chem. 264, 1329–1335.

    PubMed  CAS  Google Scholar 

  18. Clapper, D. L., Walseth, T. F., Dargie, P. J., and Lee, H. C. (1987) Pyridine nucleotide metabolites stimulate Ca2+ release from sea urchin egg microsomes desensitized to inositol trisphosphate.J. Biol. Chem. 262, 9561–9568.

    PubMed  CAS  Google Scholar 

  19. Galione, A., Lee, H. C., and Busa, W. B. (1991) Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose.Science 253, 1143–1146.

    Article  PubMed  CAS  Google Scholar 

  20. Galione, A., McDougall, A., Busa, W. B., Willmont, N., Gillot, I., and Whitaker, M. (1993) Redundant mechanisms of Ca2+ induced Ca2+ release underlying Ca2+ waves during fertilization of sea urchin eggs.Science 261, 348–352.

    Article  PubMed  CAS  Google Scholar 

  21. Lee, H. C. (1993) Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose.J. Biol. Chem. 268, 293–299.

    PubMed  CAS  Google Scholar 

  22. Lee, H. C. (1994) Cyclic ADP-ribose: a new member of a super family of signaling cyclic nucleotides.Cell Signal. 6, 591–600.

    Article  PubMed  CAS  Google Scholar 

  23. Lee, H. C., Aarhus, R., Graeff, R., Gurnack, M. E., and Walseth, T. F. (1994) Cyclic ADP-ribose activation of the ryanodine receptor is mediated by calmodulin.Nature 370, 307–309.

    Article  PubMed  CAS  Google Scholar 

  24. Lee, H. C., Aarhus, R., and Walseth, T. F. (1993) Ca2+ mobilization by dual receptor during fertilization of sea urchin eggs.Science 261, 352–355.

    Article  PubMed  CAS  Google Scholar 

  25. Aarhus, R., Dickey, D. M., Graeff, R. M., Gee, K. R., Walseth, T. F., and Lee, H. C. (1996) Activation and inactivation of Ca2+ release by NAADP+.J. Biol. Chem. 271, 8513–8516.

    Article  PubMed  CAS  Google Scholar 

  26. Gennazani, A. A., Empson, R. M., and Galione, A. (1996) Unique inactivation and activation properties of NAADP-sensitive Ca2+ release.J. Biol. Chem. 271, 11,599–12,602.

    Google Scholar 

  27. Lee, H. C. and Aarhus, R. (1995) A derivative of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADP-ribose.J. Biol. Chem. 270, 2152–2157.

    Article  PubMed  CAS  Google Scholar 

  28. Makhlouf, G. M. and Murthy, K. S. (1997) Signal transduction in gastrointestinal smooth muscle.Cell Signal. 9, 269–276.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Departments of Physiology and Medicine, Medical College of Virginia, PO Box 980711, 23298-0711, Richmond, VA

    John F. Kuemmerle, Karnam S. Murthy & Gabriel M. Makhlouf

Authors
  1. John F. Kuemmerle
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  2. Karnam S. Murthy
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  3. Gabriel M. Makhlouf
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Kuemmerle, J.F., Murthy, K.S. & Makhlouf, G.M. Longitudinal smooth muscle of the mammalian intestine. Cell Biochem Biophys 28, 31–44 (1998). https://doi.org/10.1007/BF02738308

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