Cyclic Hematopoiesis in Gray Collie Dogs

  • William P. HammondIV
  • David C. Dale


Cyclic hematopoiesis is a rare human disease for which a spontaneously occurring animal model was recognized in purebred collies in the 1960s. Initially the canine disease was called the “lethal gray syndrome” or the “silver-gray collie syndrome” because the affected collie puppies are born with gray coat color and they die prematurely. Dickson (1964) reported that the puppies die because of an absence of blood neutrophils with consequent infection. Lund et al. (1967) subsequently demonstrated that the dogs have cyclic neutropenia. In 1972, Dale et al. (1972a) reported that the reticulocytes, platelets, monocytes, eosinophils, and lymphocytes also fluctuate periodically and suggested that the name “cyclic hematopoiesis” more accurately describes this disorder.


Neutrophil Count Pluripotent Stem Cell Gray Collie Cyclical Change Reticulocyte Count 
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  1. Adamson, J. W., Dale, D. C., and Elin, R. J., 1974, Hematopoiesis in the gray collie dog. Studies of the regulation of erythropoiesis, J. Clin. Invest. 54: 965.PubMedCrossRefGoogle Scholar
  2. Angus, K., Wyand, D. S., and Yang, T. J., 1978, Impaired lymphocyte response to phytohemagglutinin in dogs affected with cyclic neutropenia, Clin. Immunol. Immunopathol. 11: 39.PubMedCrossRefGoogle Scholar
  3. Besa, E. C., Dale, D. C., Wolff, S. W., and Grdner, J. F., 1977, Aetiocholanolone and prednisolone therapy in patients with severe bone-marrow failure, Lancet 1: 728.PubMedCrossRefGoogle Scholar
  4. Cheville, N. F., 1968a, Amyloidosis associated with cyclic neutropenia in the dog, Blood 31: 111.PubMedGoogle Scholar
  5. Cheville, N. F., 1968b, The gray collie syndrome, J. Am. Vet. Med. Assoc. 152: 620.PubMedGoogle Scholar
  6. Cheville, N. F., Cutlip, R. C., and Moon, H. W., 1970, Microscopic pathology of the gray collie syndrome, Pathol. Vet. 7: 225.PubMedCrossRefGoogle Scholar
  7. Chusid, M. J., Bujak, J. S., and Dale, D. C., 1975, Defective polymorphonuclear leukocyte metabolism and function in canine cyclic neutropenia, Blood 46: 921.PubMedGoogle Scholar
  8. Dale, D. C., and Graw, R. G., Jr., 1974, Transplantation of allogeneic bone marrow in canine cyclic neutropenia, Science 183: 83.PubMedCrossRefGoogle Scholar
  9. Dale, D. C., Brown, C. H., Carbone, P, and Wolff, S. M., 1971, Cyclic urinary leukopoietic activity in gray collie dogs, Science 173: 152.PubMedCrossRefGoogle Scholar
  10. Dale, D. C., Ailing, D. W., and Wolff, S. M., 1972a, Cyclic hematopoiesis: The mechanism of cyclic neutropenia in grey collie dogs, J. Clin. Invest. 51: 2197.PubMedCrossRefGoogle Scholar
  11. Dale, D. C., Ward, S. B., Kimball, H. R. and Wolff, S. M., 1972b, Studies of neutrophil production and turnover in grey collie dogs with cyclic neutropenia, J. Clin. Invest. 51: 2190.PubMedCrossRefGoogle Scholar
  12. Deubelbeiss, K. A., Dancey, J. T., Harger, L. A., and Finch, C. A., 1975, Neutrophil kinetics in the dog, J. Clin. Invest. 55: 833.PubMedCrossRefGoogle Scholar
  13. Dickson, D. M., 1964, Early death of the silver-grey collie, Vet. Med. Small Anim. Clin. 1964: 529.Google Scholar
  14. Dunn, C. D. R., Jones, J. B., Jolly, J. D., and Lange, R. D., 1977, Progenitor cells in canine cyclic hematopoiesis, Blood 50: 1111.PubMedGoogle Scholar
  15. Dunn, C. D. R., Jolly, J. D., Jones, J. B., and Lange, R. D., 1978a, Erythroid colony formation in vitro from the marrow of dogs with cyclic hematopoiesis: Interrelationship of progenitor cells, Exp. Hematol. 6: 701.PubMedGoogle Scholar
  16. Dunn, C. D. R., Jones, J. B., Jolly, J. D., and Lange, R. D., 1978b, Cell proliferation of canine cyclic hematopoietic marrow in diffusion chambers, Proc. Soc. Exp. Biol. Med. 158: 50.PubMedGoogle Scholar
  17. Ford, L., 1958, Possible pleiotrophic effects of the gray gene in collie dogs, Proc. 10th Int. Congr. Genet. 83: 1.Google Scholar
  18. Ford, L., 1969, Hereditary aspects of human and canine cyclic neutropenia, J. Hered. 60: 293.PubMedGoogle Scholar
  19. Gregory, R. S., Machado, E. A., and Jones, J. B., 1977, Amyloidosis associated with canine cyclic hematopoiesis in the gray collie dog, Am. J. Pathol. 87: 721.PubMedGoogle Scholar
  20. Hammond, W. P., and Dale, D. C., 1980, Lithium therapy of canine cyclic hematopoiesis, Blood 55: 26.PubMedGoogle Scholar
  21. Hammond, W. P., Price, T. H., and Dale, D. C., 1978, Canine cyclic hematopoiesis: Effects of chronic endotoxin administration, Blood 52: 1170.PubMedGoogle Scholar
  22. Hammond, W. P., Engelking, E. R., and Dale, D. C., 1979, Cyclic hematopoiesis. Effects of endotoxin on colony-forming cells and colony-stimulating activity in grey collie dogs, J. Clin. Invest. 63: 785.PubMedCrossRefGoogle Scholar
  23. Jones, J. B., Yang, T. J., Dale, J. B., and Lange, R. D., 1975a, Canine cyclic hematopoiesis: Marrow transplantation between littermates, Br. J. Haematol. 30: 215.PubMedCrossRefGoogle Scholar
  24. Jones, J. B., Lange, R. D., Yang, T. J., Vodopick, H., and Jones, E. S., 1975b, Canine cyclic neutropenia: Erythropoietin and platelet cycles after bone marrow transplantation, Blood 45: 213.PubMedGoogle Scholar
  25. Lange, R. D., and Jones, J. B., 1976, Hormonal control of erythropoiesis in canine cyclic haematopoiesis, Scand. J. Haematol. 16: 56.PubMedCrossRefGoogle Scholar
  26. Lange, R. D., Jones, J. B., Chambers, C., Quirin, Y., and Sparks, J. C., 1976, Erythropoiesis and erythrocytic survival in dogs with cyclic hematopoiesis, Am. J. Vet. Res. 37: 331.PubMedGoogle Scholar
  27. Lund, J., 1969, Canine Cyclic Neutropenia, Ph.D. thesis, Washington State University.Google Scholar
  28. Lund, J. E., Padgett, G. A., and Ott, R. L., 1967, Cyclic neutropenia in grey collie dogs, Blood 29: 452.PubMedGoogle Scholar
  29. Lund, J. E., Padgett, G. A., and Gorham, J. R., 1970, Additional evidence on the inheritance of cyclic neutropenia in the dog, J. Hered. 61: 47.PubMedGoogle Scholar
  30. McDonald, T. P., Clift, R., and Jones, J. B., 1976, Canine cyclic hematopoiesis: Platelet size and thrombo-poietin level in relation to platelet count, Proc. Soc. Exp. Biol. Med. 153: 424.PubMedGoogle Scholar
  31. Machado, E. A., Gregory, R. S., Jones, J. B., and Lange, R. G., 1978, The cyclic hematopoietic dog: A model for spontaneous secondary amyloidosis, Am. J. Pathol. 92: 23.PubMedGoogle Scholar
  32. Mackey, M. C., 1978, Unified hypothesis for the origin of aplastic anemia and periodic hematopoiesis, Blood 51: 941.PubMedGoogle Scholar
  33. Maloney, M. A., Lund, J. E., and Patt, H. M., 1974, Modification of canine cyclic hematopoiesis by endotoxin, Proc. Soc. Exp. Biol. Med. 147: 205.PubMedGoogle Scholar
  34. Metcalf, D., 1977, Hemopoietic Colonies. In Vitro Cloning of Normal and Leukemic Cells, Springer-Verlag, New York.Google Scholar
  35. Morley, A. A., and Stohlman, F., Jr., 1970, Cyclophosphamide induced cyclical neutropenia, N. Engl. J. Med. 282: 643.PubMedCrossRefGoogle Scholar
  36. Patt, H. M., Lund, J. E., and Maloney, M. A., 1973, Cyclic hematopoiesis in grey collie dogs: A stem cell problem, Blood 42: 873.PubMedGoogle Scholar
  37. Reese, M. E., McDonald, T. P., and Jones, J. B., 1976, Platelet function studies in dogs with cyclic hematopoiesis, Proc. Soc. Exp. Biol. Med. 153: 324.PubMedGoogle Scholar
  38. Reynolds, H. Y., Dale, D. C., Wolff, S. M., and Johnson, J. S., 1971, Serum immunoglobulin levels in grey collies, Proc. Soc. Exp. Biol. Med. 136: 574.PubMedGoogle Scholar
  39. Scott, R. E., Dale, D. C., Rosenthal, A. S., and Wolff, S. M., 1973, Cyclic neutropenia in grey collie dogs. Ultrastructural evidence for abnormal neutrophil granulopoieses, Lab. Invest. 28: 514.PubMedGoogle Scholar
  40. Sharkis, S. J., Ahmed, A., Sensenbrenner, L. L., Jedrzejczak, W. W., and Sell, K. W., 1978, Thymic regulation of hematopoiesis: Myeloid differentiation in the stem cell defective W/Wv mouse, in: Hematopoietic Cell Differentiation (D. W. Golde, ed.), p. 491, Academic Press, New York.Google Scholar
  41. Weiden, P. L., Robinett, B., Graham, T. C., Adamson, J., and Storb, R., 1974, Canine cyclic neutropenia. A stem cell defect, J. Clin. Invest. 53: 950.PubMedCrossRefGoogle Scholar
  42. Williams, W. J., Beutler, E., Erslev, A. J., and Rundles, R. W., 1977, Hematology, McGraw-Hill, New York.Google Scholar
  43. Windhorst, D. B., Lund, J. E., Decker, J., and Swatez, I., 1967, Intestinal malabsorption in the gray collie syndrome, Fed. Proc. Fed. Am. Soc. Exp. Biol. 26: 260.Google Scholar
  44. Wintrobe, M. M., Lee, G. R., Boggs, T. C., Athens, J. W., and Foerster, J., 1974, Clinical Hematology, Lea & Febiger, Philadelphia.Google Scholar
  45. Yang, T. J., Jones, J. B., Jones, E. S., and Lange, R. D., 1974, Serum colony-stimulating activity of dogs with cyclic neutropenia, Blood 44: 41.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1981

Authors and Affiliations

  • William P. HammondIV
    • 1
  • David C. Dale
    • 1
  1. 1.Department of MedicineSchool of Medicine University of WashingtonSeattleUSA

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