Skip to main content
Log in

Diabetogenic role of insulin's counterregulatory hormones in the isletectomized, diabetic goby

  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

In an experimental model of insulin-dependent diabetes mellitus (IDDM) in the teleost fish, the goby Gillichthys mirabilis, an isletectomy procedure completely removes the pancreatic endocrine tissue without affecting the exocrine acini or other essential tissues. Interestingly, isletectomized (Ix) gobies do not exhibit a significant hyperglycemia until 10–15 d after this procedure, suggesting a lack of initial diabetogenic actions of a pancreatic factor(s). Administering exogeneous glucagon in otherwise nonsymptomatic 7-d Ix gobies, however, induces a hyperglycemic state comparable to that in severely diabetic rats or gobies (after 20 d post-Ix). The spontaneously arising hyperglycemia observed between 10 and 15d post-Ix, on the other hand, is significantly correlated with increasing serum cortisol concentrations, with both exhibiting sustained elevated levels (approx 23 mmol/L and >100 ng/mL, respectively) at 20- and 25-d post-Ix. Exogenous cortisol treatment also significantly induced hyperglycemia in nonsymptomatic, 7-d Ix gobies. By contrast, growth hormone (GH) had no detectable diabetogenic effect in 7-d Ix gobies. Serum levels of ammonia, the principal nitrogenous waste in this species, were not affected by glucagon treatment but were reduced slightly by GH treatment (30% reduction; p<0.05). Cortisol treatment, on the other hand, increased ammonia levels twofold, suggesting that the glucocorticoid induces a negative nitrogen balance. These results indicate that the counterregulatory hormones—glucagon and cortisol—are effective diabetogenic factors in the Ix goby, capable of driving metabolic imbalance in this model of IDDM.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Chang, A. Y. and Diani, A. R., (1985). In: The diabetic pancreas. Volks, B. W. and Wellmand, K. F. (eds.) Plenum: New York.

    Google Scholar 

  2. Wilson, G. L. and Leiter, E. H. (1990). Curr. Top. Microbiol. Immunol. 156, 27–54.

    PubMed  CAS  Google Scholar 

  3. Lager, I. (1991). J. Intern. Med. Suppl. 735, 41–47.

    PubMed  CAS  Google Scholar 

  4. Cryer, P. E. (1993). Am. J. Physiol. 264, E149-E155.

    PubMed  CAS  Google Scholar 

  5. De Feo, P., Perriello, G., Torlone, E., Fanelli, C., Ventura, M. M., Santeusanio, F., Brunetti, P., Gerich, J. E., and Bolli, G. B. (1991). Am. J. Physiol. 260, E203-E212.

    PubMed  Google Scholar 

  6. Smith, U., Attvall, E., Eriksson, J., Fowelin, J., Lonnroth, P., and Wesslau, C. (1993). Adv. Exp. Med. Biol. 334, 169–180.

    PubMed  CAS  Google Scholar 

  7. Raskin, P. and Unger, R. H. (1978). Med. Clin. North Am. 62, 713–722.

    PubMed  CAS  Google Scholar 

  8. Barnes, A. J., Bloom, S. R., Mashiter, K., Alberti, K. G., Smythe, P., and Turnell, D. (1977). Diabetologia 13, 71–75

    Article  PubMed  CAS  Google Scholar 

  9. Barnes, A. J., Bloom, S. R., George, K., alberti, G. M., Smythe, P., Alford, F. P., and Chisholm, D. J., (1977). N. Engl. J. Med. 296, 1250–1253.

    Article  PubMed  CAS  Google Scholar 

  10. Barnes, A. J. and Bloom, S. R. (1976). Lancet 1, 219–221.

    Article  PubMed  CAS  Google Scholar 

  11. Yasugi, H., Mizumoto, R., Sakurai, H., and Honjo, I. (1976). Am. J. Surg. 132, 577–580.

    Article  PubMed  CAS  Google Scholar 

  12. Mizumoto, R., Yano, T., Sekoguchi T., and Kawarada, Y. (1986). Int. J. Pancreatol. 1, 185–193.

    PubMed  CAS  Google Scholar 

  13. Matsuyama, T., Tanaka, R., Shima, K., and Tarui, S. (1978). Endocrinol. Jpn. 25, 529–532.

    PubMed  CAS  Google Scholar 

  14. Lussier, B. and Hetenyi, G. Jr. (1986). Can. J. Physiol. Pharmacol. 64, 1440–1442.

    PubMed  CAS  Google Scholar 

  15. Trevisan, R., Marescotti, C., Avogaro, A., Tessari, P., del Prato, S., and Tiengo, A. (1989). Diabetes. Res. 12, 57–62.

    PubMed  CAS  Google Scholar 

  16. Tiengo A., Bessioud, M., Valverde, I., Tabbi-Anneni, A., Delprato, S., Alexandre, J., and Assan, R. (1982). Diabetologia 22, 25–32.

    Article  PubMed  CAS  Google Scholar 

  17. Higuchi, A., Yasugi, H., Yokota, T., Tobe, T., and Mizumoto, R. (1979). Gastroenterol. Jpn. 14, 316–326.

    PubMed  CAS  Google Scholar 

  18. Gabel, H., Bitter-Suermann, H., Henriksson, C., Save-Soderbergh, J., Lundholm, K., and Brynger, H. (1985). Horm. Metab. Res. 17, 275–280.

    PubMed  CAS  Google Scholar 

  19. Yano, T. (1985). Nippon Geka Gakkai Zasshi 86, 470–481.

    PubMed  CAS  Google Scholar 

  20. Wilson, J. D., Dhall, D. P., Simeonovic, C. J., and Lafferty, K. J. (1986). Aust. J. Exp. Biol. Med. Sci., 64, 489–500.

    PubMed  Google Scholar 

  21. Stump, K. C., Swindle, M. M., Saudek, C. D., and Strandberg, J. D. (1988). Lab. Anim. Sci. 38, 439–443.

    PubMed  CAS  Google Scholar 

  22. Wenger, J. M., Meyer, P., Morel, D. R., Costabella, P. M., and Rohner, A. (1990). J. Surg. Res. 49, 361–365.

    Article  PubMed  CAS  Google Scholar 

  23. Dresler, C. M., Fortner, J. G., McDermott, K., and Bajorunas, D. R. (1991). Ann. Surg. 214, 131–140.

    Article  PubMed  CAS  Google Scholar 

  24. Polonsky, K. S., Herold, K. C., Gilden, J. L., Bergenstal, R. M., Fang V. S., Moossa, A. R., and Jaspan, J. B. (1984). Diabetes 33, 1112–1119.

    Article  PubMed  CAS  Google Scholar 

  25. Mizumoto, R., Kawarada, Y., Goshima, H., Tamaki, H., Sekoguchi, T., and Tomikawa, I. (1982). Am. J. Surg. 143, 237–243.

    Article  PubMed  CAS  Google Scholar 

  26. Yvi-Jarvinen, H., Kiviluoto, T., and Taskinen, M. R. (1986). Metabolism 35, 718–727.

    Article  Google Scholar 

  27. Stevenson, R. W., Williams, P. E., and Cherrington, A. D. (1987). Diabetologia 30, 782–790.

    Article  PubMed  CAS  Google Scholar 

  28. Vigili de Kreutzenberg, S., Maifreni, L., Lisato, G., Riccio, A., Trevisan, R., Tiengo, A., and del Prato, S. (1990). J. Clin. Endocrinol. Metab. 70, 1023–1029.

    PubMed  CAS  Google Scholar 

  29. Giacca, A., Fisher, S. J., McCall, R. H., Shi, Z. Q., Vranic, M. (1997). Endocrinology 138, 999–1007.

    Article  PubMed  CAS  Google Scholar 

  30. Kelley, K. M. (1993) Endocrinology 132, 2689–2695.

    Article  PubMed  CAS  Google Scholar 

  31. Kelley, K. M., Gray, E. S., Siharath, K., Nicoll, C. S., and Bern, H. A. (1993). Endocrinology 132, 2695–2701.

    Google Scholar 

  32. Kelley, K. M., Desai, P., Roth, J. T., Haigwood, J. T., Arope, S. A., Flores, R. M., Schmidt, K. E., Perez, M., Nicholson, G. S., and Song, W. W. (2000). In: Recent advances in marine biotechnology, vol. 4, Fingerman, M., Thompson, M.-F., and Nagabhushanam, R. (eds.). Oxford and IBH Publishing. New Delhi.

    Google Scholar 

  33. Kelley, K. M., Johnson, T. R., Ilan, J., and Moskowitz, R. W. (1999). Am. J. Physiol. 276, R1164-R1171.

    PubMed  CAS  Google Scholar 

  34. Sheridan, M. A. (1986). Gen. Comp. Endocrinol. 64, 220–238.

    Article  PubMed  CAS  Google Scholar 

  35. Mommsen, T. P., Danulat, E., and Walsh P. J. (1992). Opsanus beta. Gen. Comp. Endocrinol. 85, 316–326.

    Article  CAS  Google Scholar 

  36. Rodgers, B. D., Lau, A. O. T., and Nicoll, C. S. (1994) Proc. Soc. Exp. Biol. Med. 206, 220–226.

    Google Scholar 

  37. Rodgers, B. D., Strack, A. M., Dallman, M. F., Hwa, L., and Nicoll, C. S. (1995). Diabetes 44, 1420–1425.

    Article  PubMed  CAS  Google Scholar 

  38. Bates, R. W. and Garrison, M. M. (1971). Endocrinology 88, 1429–1436.

    Article  PubMed  CAS  Google Scholar 

  39. Chernick, S. S., Clark, C. M., Jr. Gardiner, R. J., and Scow, R. O., (1972). Diabetes 21, 946–954.

    PubMed  CAS  Google Scholar 

  40. Holly, J. M. P., Amiel, C. S., Sandhu, R. R., Rees, L. H. and Wass, J. A. H. (1988). J. Endocrinol. 118, 353–364.

    PubMed  CAS  Google Scholar 

  41. Leung, T. C., Ng, T. B., and Woo, N. Y. (1991). Comp. Biochem. Physiol. A 99, 633–636.

    Article  PubMed  CAS  Google Scholar 

  42. Sönkson, P. H., Russell-Jones, D., and Jones, R. H., (1993). Horm. Res. 40, 68–79.

    Google Scholar 

  43. Cryer, P. E. (1996). Horm. Res. 46, 192–194.

    PubMed  CAS  Google Scholar 

  44. Leena, S., Shameena, B., and Oommen, O. V. (1999). Endocr. Res. 25, 341–355.

    Article  PubMed  CAS  Google Scholar 

  45. Albissier, A. M., Nomura, M., Schulz, M., Bahoric, A., Kubota, M., and Holland, F. J. (1987). Horm. Metab. Res. 19, 348–352.

    Article  Google Scholar 

  46. Untermann, T. G., Jentell, J. J., Oehler, D. T., Lacson, R. G., and Hofert, J. T. (1993). Endocrinology 133, 2531–2539.

    Article  Google Scholar 

  47. Gerich, J. E. (1988). Diabetes 37, 1608–1617.

    Article  PubMed  CAS  Google Scholar 

  48. Kroncke, K. D., Fehsel, K., Sommer, A., Rodriquez, M. L., and Kolb-Bachofen, V. (1995). Biol. Chem. Hoppe Seryler 376, 179–185.

    CAS  Google Scholar 

  49. Haigwood, J. T. and Kelley, K. M. (1998). Amer. Zoologist 37, 180A.

    Google Scholar 

  50. Gray, E. S. and Kelley, K. M. (1991). J. Endocrinol. 131, 57–66.

    PubMed  CAS  Google Scholar 

  51. Umminger, B. L., Benziger, D., and Levy, S. (1975). Comp. Biochem. Physiol. 51C, 111–115.

    Google Scholar 

  52. Houssay, B. A., and Biasotti, A. (1930). Rev. Soc. Argent. Biol. 6, 251–296.

    CAS  Google Scholar 

  53. Lyall, A. and Innes, J. A. (1935). Lancet, 1, 318–319.

    Article  Google Scholar 

  54. Kollind, M., Adamson, V., Lins, P., and Efendic, S. (1987). Horm. Metab. Res. 19, 156–159.

    PubMed  CAS  Google Scholar 

  55. Kelley, K. M., Russell, S. M., Matteucci, M. L., and Nicoll, C. S. (1993). Diabetes 42, 463–469.

    Article  PubMed  CAS  Google Scholar 

  56. English, D. E., Barnum, C. L., Russell, S. M., and Nicoll, C. S. (1993). Endocr. J. 1, 73–78.

    Google Scholar 

  57. McKeown, B. A., Leatherland, J. F., and John, T. M. (1975). Comp. Biochem. Physiol. B50, 425–430.

    Article  CAS  Google Scholar 

  58. Clarke, W. C. and Bern, H. A. (1980). In: Hormonal proteins and peptides, vol. 8, Li, C. H. (eds.) Academic: New York.

    Google Scholar 

  59. Press, M., Tambourlane, W. V., and Sherwin, R. S. (1984). N. Engl. J. Med. 315, 810–815.

    Article  Google Scholar 

  60. Press, M., Tambourlane, W. V., and Sherwin, R. S. (1988). Metabolism 35, 956–959.

    Article  Google Scholar 

  61. Campbell, P. J., Bolli, G. B., Cryer, P. E., and Gerich, J. E. (1985). N. Engl. J. Med. 312, 1473–1479.

    Article  PubMed  CAS  Google Scholar 

  62. Periello, G., DeFeo, P., Torlone, E., Fanelli, C., Santeusania, F., Brunetti, P., and Bolli, G. B. (1990). Diabetologia 33, 52–59.

    Article  Google Scholar 

  63. Boyle, P. J., Avogaro, A., Smith, L., Shah, S. D., Cryer, P. E., and Santiago, J. V. (1992). Diabetologia 35, 372–379.

    Article  PubMed  CAS  Google Scholar 

  64. Pal, B. R., Phillips, P. E., Matthews, D. R., and Dunger, D. B. (1992). Diabetologia 35, 542–549.

    Article  PubMed  CAS  Google Scholar 

  65. Moller, N., Jorgensen, J. O., Moller, J., Orskov, L., Oversen, P., Schmitz, O., Christiansen, J. S., and Orskov, H. (1995). Metabolism 44, 33–36.

    Article  PubMed  CAS  Google Scholar 

  66. Schreck, C. B. (1993). In: The endocrinology of growth, depelopment, and metabolism of vertebrates. Schreibman, M. P., Scanes, C. G., and Pang, P. K. T. (eds.) Academic: San Diego.

    Google Scholar 

  67. Murat, J. C., Plisetskaya, E. M., and Woo, N. Y. S. (1981). Comp. Biochem. Physiol. 68A, 149–158.

    Article  CAS  Google Scholar 

  68. Petersen, T. D. P., Hochachka, P. W., and Suarez, P. K. (1987), J. Exp. Zool. 243, 173–180.

    Article  CAS  Google Scholar 

  69. Suarez, P. K. and Mommsen, T. P. (1987). Can. J. Zool. 65, 1869–1882.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kevin M. Kelley.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Haigwood, J.T., Flores, R.M., Mazloumi, R. et al. Diabetogenic role of insulin's counterregulatory hormones in the isletectomized, diabetic goby. Endocr 13, 273–280 (2000). https://doi.org/10.1385/ENDO:13:3:273

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1385/ENDO:13:3:273

Key Words

Navigation