OMIA:000248-9615 : Neutropenia, cyclic in Canis lupus familiaris (dog)

Categories: Haematopoietic system phene

Links to possible relevant human trait(s) and/or gene(s) in OMIM: 608233 (trait) , 603401 (gene)

Mendelian trait/disorder: yes

Mode of inheritance: Autosomal recessive

Considered a defect: yes

Key variant known: yes

Year key variant first reported: 2003

Cross-species summary: Also known as cyclic hematopoiesis and in humans as HERMANSKY-PUDLAK SYNDROME 2; HPS2

Species-specific name: Grey Collie Syndrome; Gray Collie Syndrome

Species-specific description: Cyclic neutropenia, also known as cyclic hematopoiesis or Grey/Gray Collie Syndrome, is characterized by cyclic fluctuations in the numbers of leucocytes, particularly neutrophils. Affected animals have an associated coat color dilution, producing a gray coat color. Affected dogs have cyclic reductions in leucocyte numbers, particularly neutrophils, which are associated with recurrent fever, anorexia, and severe infections, often life threatening. The mode of inheritance is autosomal recessive. Edited by Vicki N. Meyers-Wallen, VMD, PhD, Dipl. ACT

Mapping: CFA (3)

Molecular basis: By cloning and sequencing a very likely comparative candidate gene (based on the homologous human disorder), Benson et al. (2003) showed that the causative mutation is a single base pair insertion in exon 20 of AP3 beta gene (AP3B1), which encodes the beta 3A subunit of adaptor protein complex 3 (AP3). This causes a frame shift in the amino acid code, and ultimately premature termination of AP3 mRNA. Affected animals are homozygous for the mutation, have no AP3 beta mRNA, while carriers have half the expected amount (Benson et al., 2003).

Clinical features: Clinical signs are associated with severe neutropenia, and include recurrent fever, anorexia, and severe infections, which can be life threatening (Dale et al., 1972, Pacheco et al., 2008). Affected animals have an associated coat color dilution, producing a gray coat color.

Pathology: AP3 is a protein complex on the cytosolic side of membrane-bound vesicles, and directs proteins from the Golgi apparatus to lysosomes. The beta subunit of AP3 recognizes neutrophil elastase (ELA2) as its cargo and transports it to lysosomal granules. In the absence of normally functioning AP3B1, ELA2 is not transported to the correct location, and does not function properly. Neutrophils of affected dogs have elastase deficiency and accumulate elastase precursor proteins in their primary granules (Meng et al., 2010).

Prevalence: The prevalence of the mutant allele in the Collie breed is unknown. Lee et al. (2022) reported a mixed-breed puppy with the same clinical signs of this disorder as seen in Collies, and which was homozygous for the likely causal insertion variant reported in Collies (OMIA variant 580). However, the authors reported that "The puppy does not have phenotypic features suggestive of a collie and is presumed to be a cross between a Labrador Retriever and a Mastiff". Consequently, they concluded that "the AP3B1 mutation and CH are present within the general canine population and are not restricted to collies".

Control: Parents of affected dogs are carriers. Siblings of affected dogs should be tested for the causative mutation. It is recommended that carriers only be bred to noncarriers, in which case, testing of offspring is advisable.

Genetic testing: A test is available to detect the causative mutation.

Breed: Collie (Dog) (VBO_0200375).
Breeds in which the phene has been documented. (If a likely causal variant has been documented for the phene, see the variant table breeds in which the variant has been reported).

Associated gene:

Symbol Description Species Chr Location OMIA gene details page Other Links
AP3B1 adaptor-related protein complex 3, beta 1 subunit Canis lupus familiaris 3 NC_051807.1 (28405848..28672345) AP3B1 Homologene, Ensembl , NCBI gene

Variants

By default, variants are sorted chronologically by year of publication, to provide a historical perspective. Readers can re-sort on any column by clicking on the column header. Click it again to sort in a descending order. To create a multiple-field sort, hold down Shift while clicking on the second, third etc relevant column headers.

WARNING! Inclusion of a variant in this table does not automatically mean that it should be used for DNA testing. Anyone contemplating the use of any of these variants for DNA testing should examine critically the relevant evidence (especially in breeds other than the breed in which the variant was first described). If it is decided to proceed, the location and orientation of the variant sequence should be checked very carefully.

Since October 2021, OMIA includes a semiautomated lift-over pipeline to facilitate updates of genomic positions to a recent reference genome position. These changes to genomic positions are not always reflected in the ‘acknowledgements’ or ‘verbal description’ fields in this table.

OMIA Variant ID Breed(s) Variant Phenotype Gene Allele Type of Variant Source of Genetic Variant Reference Sequence Chr. g. or m. c. or n. p. Verbal Description EVA ID Year Published PubMed ID(s) Acknowledgements
580 Collie (Dog) Neutropenia, cyclic AP3B1 insertion, small (<=20) Naturally occurring variant CanFam3.1 3 g.28663129_28663130insA c.2407_2408insA p.(T803Nfs*5) NM_001002974.2; NP_001002974.1; a single base pair (A) insertion in exon 20 of the AP3 beta gene (AP3B1) 2003 12897784

Cite this entry

Nicholas, F. W., Tammen, I., & Sydney Informatics Hub. (2022). OMIA:000248-9615: Online Mendelian Inheritance in Animals (OMIA) [dataset]. https://omia.org/. https://doi.org/10.25910/2AMR-PV70

References

Note: the references are listed in reverse chronological order (from the most recent year to the earliest year), and alphabetically by first author within a year.

2023 Haginoya, S., Thomovsky, E.J., Johnson, P.A., Brooks, A.C. :
Clinical assessment of primary hemostasis: A review. Top Companion Anim Med 56-57:S1938-9736(23)00058-2:100818, 2023. Pubmed reference: 37673175. DOI: 10.1016/j.tcam.2023.100818.
2022 Lee, G.K.C., Barbosa, C., Andersen, G., Ramirez, C.J., Kornya, M., Abrams-Ogg, A., Morrison, K., Diamantino, G., Wood, R.D., Beeler-Marfisi, J., Ampuero, F., Tatiersky, L., Bienzle, D. :
Cyclic hematopoiesis in a mixed-breed dog: case report and brief review. J Vet Diagn Invest 34:1006-1009, 2022. Pubmed reference: 35904319. DOI: 10.1177/10406387221115179.
2012 Hostetter, S.J. :
Neutrophil function in small animals. Vet Clin North Am Small Anim Pract 42:157-71, 2012. Pubmed reference: 22285163. DOI: 10.1016/j.cvsm.2011.09.010.
Yanay, O., Dale, D.C., Osborne, W.R. :
Repeated lentivirus-mediated granulocyte colony-stimulating factor administration to treat canine cyclic neutropenia. Hum Gene Ther 23:1136-43, 2012. Pubmed reference: 22845776. DOI: 10.1089/hum.2012.045.
2010 Meng, R., Bridgman, R., Toivio-Kinnucan, M., Niemeyer, GP., Vernau, W., Hock, T., Lothrop, CD. :
Neutrophil elastase-processing defect in cyclic hematopoietic dogs. Exp Hematol 38:104-15, 2010. Pubmed reference: 19941936. DOI: 10.1016/j.exphem.2009.09.010.
2009 Newburger, P.E. :
Cyclic neutropenia in animals. Am J Hematol 84:258; author reply 258, 2009. Pubmed reference: 19208418. DOI: 10.1002/ajh.21356.
2008 Pacheco, J.M., Traulsen, A., Antal, T., Dingli, D. :
Cyclic neutropenia in mammals. Am J Hematol 83:920-1, 2008. Pubmed reference: 18951469. DOI: 10.1002/ajh.21295.
2007 Horwitz, M.S., Duan, Z., Korkmaz, B., Lee, H.H., Mealiffe, M.E., Salipante, S.J. :
Neutrophil elastase in cyclic and severe congenital neutropenia. Blood 109:1817-24, 2007. Pubmed reference: 17053055. DOI: 10.1182/blood-2006-08-019166.
2006 Yanay, O., Brzezinski, M., Christensen, J., Liggitt, D., Dale, D.C., Osborne, W.R. :
An adult dog with cyclic neutropenia treated by lentivirus- mediated delivery of granulocyte colony-stimulating factor. Hum Gene Ther 17:464-9, 2006. Pubmed reference: 16610934. DOI: 10.1089/hum.2006.17.464.
2004 Benson, KF., Person, RE., Li, FQ., Williams, K., Horwitz, M. :
Paradoxical homozygous expression from heterozygotes and heterozygous expression from homozygotes as a consequence of transcriptional infidelity through a polyadenine tract in the AP3B1 gene responsible for canine cyclic neutropenia. Nucleic Acids Res 32:6327-33, 2004. Pubmed reference: 15576359. DOI: 10.1093/nar/gkh974.
Horwitz, M., Benson, KF., Duan, Z., Li, FQ., Person, RE. :
Hereditary neutropenia: dogs explain human neutrophil elastase mutations. Trends Mol Med 10:163-70, 2004. Pubmed reference: 15059607. DOI: 10.1016/j.molmed.2004.02.002.
2003 Benson, K.F., Li, F.Q., Person, R.E., Albani, D., Duan, Z., Wechsler, J., Meade-White, K., Williams, K., Acland, G.M., Niemeyer, G., Lothrop, C.D., Horwitz, M. :
Mutations associated with neutropenia in dogs and humans disrupt intracellular transport of neutrophil elastase Nature Genetics 35:90-6, 2003. Pubmed reference: 12897784. DOI: 10.1038/ng1224.
Yanay, O., Barry, S.C., Katen, L.J., Brzezinski, M., Flint, L.Y., Christensen, J., Liggitt, D., Dale, D.C., Osborne, W.R. :
Treatment of canine cyclic neutropenia by lentivirus-mediated G-CSF delivery Blood 102:2046-52, 2003. Pubmed reference: 12750178. DOI: 10.1182/blood-2002-12-3722.
1996 Allen, W.M., Pocock, P.I., Dalton, P.M., Richards, H.E., Aitken, M.M. :
Cyclic neutropenia in Collies Veterinary Record 138:371-372, 1996. Pubmed reference: 8737267.
1995 Brabb, T., Maggioprice, L., Dale, D., Deeb, B., Liggitt, D. :
Pancreatic adenocarcinoma in two grey collie dogs with cyclic hematopoiesis Laboratory Animal Science 45:357-362, 1995. Pubmed reference: 7474871.
Dale, D.C., Rodger, E., Cebon, J., Ramesh, N., Hammond, W.P., Zsebo, K.M. :
Long-term treatment of canine cyclic hematopoiesis with recombinant canine stem cell factor. Blood 85:74-9, 1995. Pubmed reference: 7528575.
1994 Avalos, B.R., Broudy, V.C., Ceselski, S.K., Druker, B.J., Griffin, J.D., Hammond, W.P. :
Abnormal response to granulocyte colony-stimulating factor (G-CSF) in canine cyclic hematopoiesis is not caused by altered G-CSF receptor expression. Blood 84:789-94, 1994. Pubmed reference: 7519075.
1992 Mishu, L., Callahan, G., Allebban, Z., Maddux, J.M., Boone, T.C., Souza, L.M., Lothrop, C.D. :
Effects of recombinant canine granulocyte colony-stimulating factor on white blood cell production in clinically normal and neutropenic dogs. J Am Vet Med Assoc 200:1957-64, 1992. Pubmed reference: 1379221.
1991 Lothrop, C.D., Candler, R.V., Pratt, H.L., Urso, I.M., Jones, J.B., Carroll, R.C. :
Characterization of Platelet Function in Cyclic Hematopoietic Dogs Experimental Hematology 19:916-922, 1991. Pubmed reference: 1893969.
1990 Moazed, T.C., Deeb, B.J., DiGiacomo, R.F. :
Subcutaneous abscess due to Salmonella adelaide in a grey collie with cyclic hematopoiesis. Lab Anim Sci 40:639-41, 1990. Pubmed reference: 2172633.
Pratt, H.L., Carroll, R.C., McClendon, S., Smathers, E.C., Souza, L.M., Lothrop, C.D. :
Effects of recombinant granulocyte colony-stimulating factor treatment on hematopoietic cycles and cellular defects associated with canine cyclic hematopoiesis. Exp Hematol 18:1199-203, 1990. Pubmed reference: 1699776.
1988 Abkowitz, J.L., Holly, R.D., Hammond, W.P. :
Cyclic hematopoiesis in dogs: studies of erythroid burst-forming cells confirm an early stem cell defect. Exp Hematol 16:941-5, 1988. Pubmed reference: 3181344.
Eglitis, M.A., Kantoff, P.W., Jolly, J.D., Jones, J.B., Anderson, W.F., Lothrop, C.D. :
Gene transfer into hematopoietic progenitor cells from normal and cyclic hematopoietic dogs using retroviral vectors. Blood 71:717-22, 1988. Pubmed reference: 2830927.
Lothrop, C.D., Warren, D.J., Souza, L.M., Jones, J.B., Moore, M.A. :
Correction of canine cyclic hematopoiesis with recombinant human granulocyte colony-stimulating factor. Blood 72:1324-8, 1988. Pubmed reference: 2458781.
1987 Al-Lebban, Z.S., Lange, R.D., Jones, J.B., Lothrop, C.D. :
Long-term bone marrow culture systems: normal and cyclic hematopoietic dogs. Can J Vet Res 51:162-8, 1987. Pubmed reference: 3607647.
Hammond, W.P., Rodger, E.R., Dale, D.C. :
Lithium augments GM-CSA generation in canine cyclic hematopoiesis. Blood 69:117-23, 1987. Pubmed reference: 3491636.
Lothrop, C.D., Coulson, P.A., Nolan, H.L., Cole, B., Jones, J.B., Sanders, W.L. :
Cyclic hormonogenesis in gray collie dogs: interactions of hematopoietic and endocrine systems. Endocrinology 120:1027-32, 1987. Pubmed reference: 3026784. DOI: 10.1210/endo-120-3-1027.
Yang, T.J. :
Pathobiology of canine cyclic hematopoiesis (review). In Vivo 1:297-302, 1987. Pubmed reference: 2979797.
1986 Trail, P.A., Yang, T.J. :
Canine cyclic hematopoiesis: alterations in T lymphocyte subpopulations in peripheral blood, lymph nodes, and thymus of gray collie dogs. Clin Immunol Immunopathol 41:216-26, 1986. Pubmed reference: 2945680. DOI: 10.1016/0090-1229(86)90105-4.
1985 Boney, C.M., McDonald, T.P., Jones, J.B. :
Abnormal function and thromboxane release from platelets of dogs with cyclic hematopoiesis. Exp Hematol 13:586-90, 1985. Pubmed reference: 3996494.
1984 Jones, J.B., Painter, P.C., Jolly, J.D., Lange, R.D. :
Nucleotide and prostaglandin cycling in canine cyclic hematopoiesis. Proc Soc Exp Biol Med 177:392-8, 1984. Pubmed reference: 6096876. DOI: 10.3181/00379727-177-41962.
Trail, P.A., Yang, T.J., Cameron, J.A. :
Increase in the haemolytic complement activity of dogs affected with cyclic haematopoiesis. Vet Immunol Immunopathol 7:359-68, 1984. Pubmed reference: 6506453. DOI: 10.1016/0165-2427(84)90093-x.
1983 DiGiacomo, R.F., Hammond, W.P., Kunz, L.L., Cox, P.A. :
Clinical and pathologic features of cyclic hematopoiesis in grey collie dogs. Am J Pathol 111:224-33, 1983. Pubmed reference: 6846503.
Hammond, W.P., Robertson, R.P., Dale, D.C. :
Mechanism of canine cyclic hematopoiesis: the role of prostaglandin E in feedback regulation. Am J Hematol 14:27-36, 1983. Pubmed reference: 6837566. DOI: 10.1002/ajh.2830140104.
Jones, J.B., Lange, R.D. :
Cyclic Hematopoiesis: animal models. Exp Hematol 11:571-80, 1983. Pubmed reference: 6884440.
Osborne, W.R., Hammond, W.P., Dale, D.C. :
Canine cyclic hematopoiesis is associated with abnormal purine and pyrimidine metabolism. J Clin Invest 71:1348-55, 1983. Pubmed reference: 6853718. DOI: 10.1172/jci110887.
1982 Dunn, C.D., Jones, J.B., Lange, R.D., Wright, E.G., Moore, M.A. :
Production of presumptive humoral haematopoietic regulators in canine cyclic haematopoiesis. Cell Tissue Kinet 15:1-10, 1982. Pubmed reference: 7060078. DOI: 10.1111/j.1365-2184.1982.tb01018.x.
Hammond, W.P., Dale, D.C. :
Cyclic hematopoiesis: effects of lithium on colony-forming cells and colony-stimulating activity in grey collie dogs. Blood 59:179-84, 1982. Pubmed reference: 6976196.
Hammond, W.P., Adamson, J.W., Dale, D.C. :
Canine cyclic haematopoiesis: the effect of endotoxin on erythropoiesis. Br J Haematol 50:283-94, 1982. Pubmed reference: 7059519. DOI: 10.1111/j.1365-2141.1982.tb01918.x.
Jones, J.B., Jolly, J.D. :
Canine cyclic haematopoiesis: bone marrow adherent cell influence of CFU-C formation. Br J Haematol 50:607-17, 1982. Pubmed reference: 7066210. DOI: 10.1111/j.1365-2141.1982.tb01961.x.
Kraisha, S., Andrews, R.B., Evans, J.H., Jones, J.B., Lange, R.D. :
Canine cyclic hematopoiesis: blood gas and 2,3-diphosphoglyceric acid studies. Am J Vet Res 43:528-30, 1982. Pubmed reference: 6803622.
Yang, T.J., Yoshida, T., Kim, S.N., Jones, J.B. :
Increase in the serum macrophage migration inhibitory activity and lysozyme in dogs affected with cyclic hematopoiesis. Exp Hematol 10:867-73, 1982. Pubmed reference: 6759148.
1981 Machado, E.A., Jones, J.B., Aggio, M.C., Chernoff, A.I., Maxwell, P.A., Lange, R.D. :
Ultrastructural changes of bone marrow in canine cyclic hematopoiesis (CH dog). A sequential study. Virchows Arch A Pathol Anat Histol 390:93-108, 1981. Pubmed reference: 7281477. DOI: 10.1007/BF00443900.
Wyand, R.C., Yang, T.J. :
T and B lymphocyte levels in the peripheral blood of dogs affected with cyclic neutropenia. Exp Hematol 9:52-62, 1981. Pubmed reference: 6972315.
1980 Hammond, W.P., Dale, D.C. :
Lithium treatment of cyclic hematopoiesis in the gray collie. Adv Exp Med Biol 127:167-73, 1980. Pubmed reference: 7405719. DOI: 10.1007/978-1-4757-0259-0_12.
Hammond, W.P., Dale, D.C. :
Lithium therapy of canine cyclic hematopoiesis. Blood 55:26-8, 1980. Pubmed reference: 7350939.
Matsas, D.J., Yang, T.J. :
Karyotype analysis of leukocytes of gray collie (cyclic neutropenia)-normal bone marrow transplant chimeras six years after transplantation. Am J Vet Res 41:1863-4, 1980. Pubmed reference: 7011123.
1979 Hammond, W.P., Engelking, E.R., Dale, D.C. :
Cyclic hematopoiesis. Effects of endotoxin on colony-forming cells and colony-stimulating activity in grey collie dogs. J Clin Invest 63:785-92, 1979. Pubmed reference: 438337. DOI: 10.1172/JCI109363.
1978 Angus, K., Wyand, D.S., Yang, T.J. :
Impaired lymphocyte response to phytohemagglutinin in dogs affected with cyclic neutropenia. Clin Immunol Immunopathol 11:39-51, 1978. Pubmed reference: 568046. DOI: 10.1016/0090-1229(78)90202-7.
Angus, K., Yang, T.J. :
Elevated autorosette formation by lymphocytes of dogs affectd with cyclic neutropenia (CN). Immunology 35:1005-8, 1978. Pubmed reference: 738763.
Dunn, C.D., Jolly, J.D., Jones, J.B., Lange, R.D. :
Erythroid colony formation in vitro from the marrow of dogs with cyclic hematopoiesis: interrelationship of progenitor cells. Exp Hematol 6:701-8, 1978. Pubmed reference: 710550.
Dunn, C.D.R., Jones, J.B., Jolly, J.D., Lange, R.D. :
Cell proliferation of canine cyclic hematopoietic marrow in diffusion chambers Proceedings of the Society for Experimental Biology and Medicine 158:50-53, 1978. Pubmed reference: 351627.
Hammond, W.P., Price, T.H., Dale, D.C. :
Canine cyclic hematopoiesis: effects of chronic endotoxin administration. Blood 52:1170-7, 1978. Pubmed reference: 719169.
Machado, E.A., Gregory, R.S., Jones, J.B., Lange, R.D. :
The cyclic hematopoietic dog: a model for spontaneous secondary amyloidosis. A morphologic study. Am J Pathol 92:23-34, 1978. Pubmed reference: 686147.
White, J.F., Jones, J.B., Lange, R.D., Fuhr, J.E. :
Evidence for the existence of an agent in the serum of the cyclic hematopoietic dog which influences hemoglobin synthesis. Experientia 34:1367-8, 1978. Pubmed reference: 738429. DOI: 10.1007/BF01981478.
Yang, T.J. :
Recovery of hair coat colour in Gray Collie (cyclic neutropenia) normal bone marrow transplant chimeras American Journal of Pathology 91:149-153, 1978. Pubmed reference: 347941.
1977 Dunn, C.D., Jones, J.B., Jolly, J.D., Lange, R.D. :
Progenitor cells in canine cyclic hematopoiesis. Blood 50:1111-20, 1977. Pubmed reference: 336117.
1976 Lange, R.D., Jones, J.B. :
Hormonal control of erythropoiesis in canine cyclic haematopoiesis. Scand J Haematol 16:56-65, 1976. Pubmed reference: 1251140. DOI: 10.1111/j.1600-0609.1976.tb01117.x.
Lange, R.D., Jones, J.B., Chambers, C., Quirin, Y., Sparks, J.C. :
Erythropoiesis and erythrocytic survival in dogs with cyclic hematopoiesis. Am J Vet Res 37:331-4, 1976. Pubmed reference: 1259228.
McDonald, T.P., Clift, R., Jones, J.B. :
Canine cyclic hematopoiesis: platelet size and thrombopoietin level in relation to platelet count. Proc Soc Exp Biol Med 153:424-8, 1976. Pubmed reference: 1013155. DOI: 10.3181/00379727-153-39561.
Reese, M.E., McDonald, T.P., Jones, J.B. :
Platelet function studies in dogs with cyclic hematopoiesis. Proc Soc Exp Biol Med 153:324-9, 1976. Pubmed reference: 995965. DOI: 10.3181/00379727-153-39538.
Yang, T.J., Dale, J.B., Jones, J.B. :
Cyclic activity of DNA synthesis of peripheral blood leukocytes in canine cyclic neutropenia. Exp Mol Pathol 25:121-30, 1976. Pubmed reference: 955040. DOI: 10.1016/0014-4800(76)90022-8.
1975 Cheville, N.F. :
The Grey Collie syndrome (cyclic neutropenia) Journal of the American Animal Hospital Association 11:350-352, 1975.
Chusid, M.J., Bujak, J.S., Dale, D.C. :
Defective polymorphonuclear leukocyte metabolism and function in canine cyclic neutropenia. Blood 46:921-30, 1975. Pubmed reference: 173440.
Jones, J.B., Lange, R.D., Jones, E.S. :
Cyclic hematopoiesis in a colony of dogs. J Am Vet Med Assoc 166:365-7, 1975. Pubmed reference: 1167851.
Jones, J.B., Lange, R.D., Yang, T.J., Vodopick, H., Jones, E.S. :
Canine cyclic neutropenia: Erythropoietin and platelet cycles after bone marrow transplantation. Blood 45:213-9, 1975. Pubmed reference: 47249.
Jones, J.B., Yang, T.J., Dale, J.B., Lange, R.D. :
Canine cyclic haematopoiesis: marrow transplantation between littermates. Br J Haematol 30:215-23, 1975. Pubmed reference: 127610. DOI: 10.1111/j.1365-2141.1975.tb00535.x.
1974 Adamson, J.W., Dale, D.C., Elm, R.J. :
Hematopoiesis in the Grey Collie dog : studies of the regulation of erythropoiesis Journal of Clinical Investigation 54:965-973, 1974. Pubmed reference: 4430726. DOI: 10.1172/JCI107837.
Adamson, J.W., Dale, D.C., Elm, R.J. :
Regulation of cyclic erthropoiesis in the Grey Collie Journal of Clinical Investigation 52:1A abstract, 1974.
Dale, D.C., Graw, R.G. :
Transplantation of allogenic bone marrow in canine cyclic neutropenia. Science 183:83-4, 1974. Pubmed reference: 4587264. DOI: 10.1126/science.183.4120.83.
Maloney, M.A., Lund, J.E., Patt, H.M. :
Modification of canine cyclic hematopoiesis by endotoxin. Proc Soc Exp Biol Med 147:205-10, 1974. Pubmed reference: 4612548. DOI: 10.3181/00379727-147-38312.
Weiden, P.L., Robinett, B., Graham, T.C., Adamson, J., Storb, R. :
Canine cyclic neutropenia. A stem cell defect. J Clin Invest 53:950-3, 1974. Pubmed reference: 4591036. DOI: 10.1172/JCI107636.
Yang, T.J., Jones, J.B., Jones, E.S., Lange, R.D. :
Serum colony-stimulating activity of dogs with cyclic neutropenia. Blood 44:41-8, 1974. Pubmed reference: 4834515.
1973 Lund, J.E., Gordon, J.R., Padgett, G.A. :
Canine cyclic neutropenia. Mod Vet Pract 54:63-5, 1973. Pubmed reference: 4795953.
Patt, H.M., Lund, J.E., Maloney, M.A. :
Cyclic hematopoiesis in grey Collie dogs: a stem cell problem Blood 42:873-884, 1973. Pubmed reference: 4796766.
Scott, R.E., Dale, D.C., Rosenthal, A.S., Wolff, S.M. :
Cyclic neutropenia in grey collie dogs. Ultrastructural evidence for abnormal neutrophil granulopoiesis. Lab Invest 28:514-25, 1973. Pubmed reference: 4703853.
1972 Dale, D.C., Alling, D.W., Wolff, S.M. :
Cyclic hematopoiesis: the mechanism of cyclic neutropenia in Grey Collie dogs Journal of Clinical Investigation 51:2197-2204, 1972. Pubmed reference: 5054472. DOI: 10.1172/JCI107027.
Dale, D.C., Ward, S.B., Kimball, H.R., Wolff, S.M. :
Studies of neutrophil production and turnover in gray Collie dogs with cyclic neutropenia Journal of Clinical Investigation 51:2190-2196, 1972. Pubmed reference: 5054471.
1971 Dale, D.C., Brown, C.H., Carbone, P., Wolff, S.M. :
Cyclic urinary leukopoietic activity in gray collie dogs. Science 173:152-3, 1971. Pubmed reference: 5581910. DOI: 10.1126/science.173.3992.152.
Reynold, H.Y., Dale, D.C., Wolff, S.M., Johnson, J.S. :
Serum immunoglobulin levels in Grey Collies Society for Experimental Biology and Medicine 136:574-577, 1971.
1970 Cheville, N.F., Cutlip, R.C., Moon, H.W. :
Microscopic pathology of the gray collie syndrome. Cyclic neutropenia, amyloidosis, enteritis, and bone necrosis. Pathol Vet 7:225-45, 1970. Pubmed reference: 5534257. DOI: 10.1177/030098587000700302.
Lund, J.E., Padgett, G.A., Gorham, J.R. :
Additional evidence on the inheritance of cyclic neutropenia in the dog. J Hered 61:47-9, 1970. Pubmed reference: 5529685. DOI: 10.1093/oxfordjournals.jhered.a108033.
1969 Ford, L. :
Hereditary aspects of human and canine cyclic neutropenia. J Hered 60:293-9, 1969. Pubmed reference: 5366324. DOI: 10.1093/oxfordjournals.jhered.a107998.
1968 Cheville, N.F. :
Amyloidosis associated with cyclic neutropenia in the dog. Blood 31:111-4, 1968. Pubmed reference: 4170467.
1967 Lund, J.E., Padgett, G.A., Ott, R.L. :
Cyclic neutropenia in grey collie dogs. Blood 29:452-61, 1967. Pubmed reference: 6067150.

Edit History


  • Created by Frank Nicholas on 20 Nov 2010
  • Changed by Martha MaloneyHuss on 18 Aug 2011
  • Changed by Vicki Meyers-Wallen on 10 Sep 2011
  • Changed by Frank Nicholas on 12 Dec 2011
  • Changed by Frank Nicholas on 21 Sep 2012
  • Changed by Frank Nicholas on 26 Jan 2013
  • Changed by Frank Nicholas on 22 Aug 2022