Isolation and characterization of pediatric canine bone marrow CD34 + cells

Veterinary Immunology and Immunopathology

Volumn 101, Issue 1-2, 2004, Pages 31-47

  Suter, Steven E ^a,c   Gouthro, Terry A ^a   McSweeney, Peter A ^b,d   Nash, Richard A ^b   Haskins, Mark E ^a   Felsburg, Peter J ^a   Henthorn, Paula S ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

BM; BMMC; bone marrow; bone marrow mononuclear cells; canine granulocyte colony stimulating factor; canine stem cell factor; CB; cG CSF; cord blood; cSCF; dog serum; DPBS; DS; Dulbecco's phosphate buffer saline without CaCl2 or MgCl2; epo

Indexed keywords

CD34 ANTIGEN; FLT3 LIGAND; MESSENGER RNA; METHYLCELLULOSE; STEM CELL FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CELL ACTIVITY; CELL COUNT; CELL CULTURE; CELL ISOLATION; CELL POPULATION; CELL SUSPENSION; COLONY FORMING UNIT GM; CONTROLLED STUDY; DOG; ENZYME ASSAY; FEMALE; GENE TRANSFER; IN VITRO STUDY; IN VIVO STUDY; IRRADIATION; LYMPHOID CELL; MALE; NONHUMAN; ONTOGENY;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD34; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELL DIVISION; CYSTATINS; DOGS; FEMALE; GENES, SRY; IMMUNOMAGNETIC SEPARATION; MALE; PROTO-ONCOGENE PROTEINS C-KIT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SEVERE COMBINED IMMUNODEFICIENCY;

ANIMALIA; CANIS FAMILIARIS; SIGANUS;

EID: 3142604748     PISSN: 01652427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetimm.2004.03.009     Document Type: Article

References (84)

1. + cells selected by immunomagnetic procedures in patients with multiple myeloma. Bone Marrow Transpl. 22:1998;957-963
2. al-Lebban Z.S., Henry J.M., Jones J.B., Eglitis M.A., Anderson W.F., Lothrop C.D. Jr. Increased efficiency of gene transfer with retroviral vectors in neonatal hematopoietic progenitor cells. Exp. Hematol. 18:1990;180-184
3. Allen J.E., Henshaw D.L. An in situ study of CD34(+) cells in human fetal bone marrow. Br. J. Haematol. 114:2001;201-210
4. + marrow cells, devoid of T and B lymphocytes, reconstitute stable lymphopoiesis and myelopoiesis in lethally irradiated allogeneic baboons. Blood. 80:1992;1693-1701
5. + peripheral blood stem cells (PBSC) in patients with advanced hematologic malignancy. Bone Marrow Transpl. 17(Suppl 2):1996;38-39
6. + marrow cells engraft lethally irradiated baboons. J. Clin. Invest. 81:1988;951-955
7. Bousso P., Wahn V., Douagi I., Horneff G., Pannetier C., Le Deist F., Zepp F., Niehues T., Kourilsky P., Fischer A., de Saint Basile G. Diversity, functionality, and stability of the T cell repertoire derived in vivo from a single human T cell precursor. Proc. Nat. Acad. Sci. USA. 97:2000;274-278
8. + selected bone marrow grafts are radioprotective and establish mixed chimerism in dogs given high dose total body irradiation. Transplantation. 68:1999;338-344
9. Buckley R.H., Schiff S.E., Schiff R.I., Markert L., Williams L.W., Roberts J.L., Myers L.A., Ward F.E. Hematopoietic stem-cell transplantation for the treatment of severe combined immunodeficiency. N. Engl. J. Med. 340:1999;508-516
10. Cornetta K., Gharpure V., Mills B., Hromas R., Abonour R., Broun E.R., Traycoff C.M., Hanna M., Wyman N., Danielson C., Gonin R., Kunkel L.K., Oldham F., Srour E.F. Rapid engraftment after allogeneic transplantation using CD34-enriched marrow cells. Bone Marrow Transpl. 21:1998;65-71
11. Dale D.C., Nichol J.L., Rich D.A., Best D.M., Slichter S.J., Sheridan W., Hunt P. Chronic thrombocytopenia is induced in dogs by development of cross-reacting antibodies to the MpL ligand. Blood. 90:1997;3456-3461
12. Dao M.A., Arevalo J., Nolta J.A. Reversibility of CD34 expression on human hematopoietic stem cells that retain the capacity for secondary reconstitution. Blood. 101:2003;112-118
13. D'Arena G., Savino L., Nunziata G., Cascavilla N., Matera R., Pistolese G., Carella A.M. Immunophenotypic profile of AC133-positive cells in bone marrow, mobilized peripheral blood and umbilical cord blood. Leukemia Lymphoma. 43:2002;869-873
14. de Haan G., Szilvassy S.J., Meyerrose T.E., Dontje B., Grimes B., Van Zant G. Distinct functional properties of highly purified hematopoietic stem cells from mouse strains differing in stem cell numbers. Blood. 96:2000;1374-1379
15. de Haan G., Van Zant G. Dynamic changes in mouse hematopoietic stem cell numbers during aging. Blood. 93:1999;3294-3301
16. + marrow cell population is multipotential. Cells Tissues Organs. 170:2002;73-82
17. - cells expressing Flk2/Flt3. Br. J. Haematol. 119:2002;525-534
18. Felsburg P.J., Hartnett B.J., Henthorn P.S., Moore P.F., Krakowka S., Ochs H.D. Canine X-linked severe combined immunodeficiency. Vet. Immunol. Immunopathol. 69:1999;127-135
19. Felsburg P.J., Somberg R.L., Hartnett B.J., Henthorn P.S., Carding S.R. Canine X-linked severe combined immunodeficiency: a model for investigating the requirement for the common gamma chain (gamma c) in human lymphocyte development and function. Immunol. Res. 17:1998;63-73
20. Felsburg P.J., Somberg R.L., Hartnett B.J., Suter S.F., Henthorn P.S., Moore P.F., Weinberg K.I., Ochs H.D. Full immunologic reconstitution following nonconditioned bone marrow transplantation for canine X-linked severe combined immunodeficiency. Blood. 90:1997;3214-3221
21. Fina L., Molgaard H.V., Robertson D., Bradley N.J., Monaghan P., Delia D., Sutherland D.R., Baker M.A., Greaves M.F. Expression of the CD34 gene in vascular endothelial cells. Blood. 75:1990;2417-2426
22. Gebhard D.H., Carter P.B. Identification of canine T-lymphocyte subsets with monoclonal antibodies. Vet. Immunol. Immunopathol. 33:1992;187-199
23. Geiger H., True J.M., de Haan G., Van Zant G. Age- and stage-specific regulation patterns in the hematopoietic stem cell hierarchy. Blood. 98:2001;2966-2972
24. Glickman L.T., Domanski L.M. An alternative to laboratory animal experimentation for human health risk assessment: epidemiological studies of pet animals. ATLA. 13:1986;267-285
25. Gluckman E., Broxmeyer H.A., Auerbach A.D., Friedman H.S., Douglas G.W., Devergie A., Esperou H., Thierry D., Socie G., Lehn P. Hematopoietic reconstitution in a patient with Fanconi's anemia by means of umbilical-cord blood from an HLA-identical sibling. N. Engl. J. Med. 321:1989;1174-1178
26. Golfier F., Barcena A., Harrison M.R., Muench M.O. Fetal bone marrow as a source of stem cells for in utero or postnatal transplantation. Br. J. Haematol. 109:2000;173-181
27. Goodell M.A., Brose K., Paradis G., Conner A.S., Mulligan R.C. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 183:1996;1797-1806
28. Goodell M.A., Rosenzweig M., Kim H., Marks D.F., DeMaria M., Paradis G., Grupp S.A., Sieff C.A., Mulligan R.C., Johnson R.P. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat. Med. 3:1997;1337-1345
29. Haddad E., Le Deist F., Aucouturier P., Cavazzana-Calvo M., Blanche S., De Saint Basile G., Fischer A. Long-term chimerism and B-cell function after bone marrow transplantation in patients with severe combined immunodeficiency with B cells: a single-center study of 22 patients. Blood. 94:1999;2923-2930
30. - cells in cord blood and bone marrow. Blood. 86:1995;3745-3753
31. Hartnett B.J., Henthorn P.S., Moore P.F., Weinberg K.I., Ochs H.D., Felsburg P.J. Bone marrow transplantation for canine X-linked severe combined immunodeficiency. Vet. Immunol. Immunopathol. 69:1999;137-144
32. + bone marrow cells. Biol. Blood Marrow Transpl. 8:2002;188-197
33. Henthorn P.S., Somberg R.L., Fimiani V.M., Puck J.M., Patterson D.F., Felsburg P.J. IL-2R gamma gene microdeletion demonstrates that canine X-linked severe combined immunodeficiency is a homologue of the human disease. Genomics. 23:1994;69-74
34. Holyoake T.L., Nicolini F.E., Eaves C.J. Functional differences between transplantable human hematopoietic stem cells from fetal liver, cord blood, and adult marrow. Exp. Hematol. 27:1999;1418-1427
35. Hows J.M. Status of umbilical cord blood transplantation in the year 2001. J. Clin. Pathol. 54:2001;428-434
36. - hematopoietic stem cells. Blood. 83:1994;1515-1526
37. Jezyk P.F., Felsburg P.J., Haskins M.E., Patterson D.F. X-linked severe combined immunodeficiency in the dog. Clin. Immunol. Immunopathol. 52:1989;173-189
38. Jordan C.T., Astle C.M., Zawadzki J., Mackarehtschian K., Lemischka I.R., Harrison D.E. Long-term repopulating abilities of enriched fetal liver stem cells measured by competitive repopulation. Exp. Hematol. 23:1995;1011-1015
39. Kessinger A., Armitage J.O., Landmark J.D., Smith D.M., Weisenburger D.D. Autologous peripheral hematopoietic stem cell transplantation restores hematopoietic function following marrow ablative therapy. Blood. 71:1988;723-727
40. Kiem H.P., Andrews R.G., Morris J., Peterson L., Heyward S., Allen J.M., Rasko J.E., Potter J., Miller A.D. Improved gene transfer into baboon marrow repopulating cells using recombinant human fibronectin fragment CH-296 in combination with interleukin-6, stem cell factor, FLT-3 ligand, and megakaryocyte growth and development factor. Blood. 92:1998;1878-1886
41. Kong S.S., Knapp J., Selvaggi G., Kenyon N.S., Ricordi C. Characterization of pediatric vertebral bone marrow. Transpl. Proc. 29:1997;1955
42. Krause D.S., Ito T., Fackler M.J., Smith O.M., Collector M.I., Sharkis S.J., May W.S. Characterization of murine CD34, a marker for hematopoietic progenitor and stem cells. Blood. 84:1994;691-701
43. - stem cells that give rise to SCID-repopulating cells. Blood. 101:2003;869-876
44. Ladiges W.C., Storb R., Thomas E.D. Canine models of bone marrow transplantation. Lab. Anim. Sci. 40:1990;11-15
45. Lansdorp P.M., Dragowska W., Mayani H. Ontogeny-related changes in proliferative potential of human hematopoietic cells. J. Exp. Med. 178:1993;787-791
46. Lanza F., Campioni D., Moretti S., Dominici M., Punturieri M., Focarile E., Pauli S., Dabusti M., Tieghi A., Bacilieri M., Scapoli C., De Angeli C., Galluccio L., Castoldi G. CD34(+) cell subsets and long-term culture colony-forming cells evaluated on both autologous and normal bone marrow stroma predict long-term hematopoietic engraftment in patients undergoing autologous peripheral blood stem cell transplantation. Exp. Hematol. 29:2001;1484-1493
47. Larochelle A., Vormoor J., Hanenberg H., Wang J.C., Bhatia M., Lapidot T., Moritz T., Murdoch B., Xiao X.L., Kato I., Williams D.A., Dick J.E. Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implications for gene therapy. Nat. Med. 2:1996;1329-1337
48. Laughlin M.J., Christiansen N.P., Herzig G.P., Blumenson L., Bonney D., Stewart C.C. CD34 progenitor cell subset analyses in normal human bone marrow and marrow harvested after intermediate-dose chemotherapy. Cytometry. 26:1996;235-242
49. Lian Z., Toki J., Yu C., Hayashi H., Yasumizu R., Sugiura K., Jin T., Inaba M., Hisha H., Li Y., Yu W., Fan H., Ikehara S. Intrathymically injected hematopoietic stem cells can differentiate into all lineage cells in the thymus: differences between c-kit+ cells and c-kit< low cells. Stem Cells. 15:1997;430-436
50. Liu H., Verfaillie C.M. Myeloid-lymphoid initiating cells (ML-IC) are highly enriched in the rhodamine-c-kit(+)CD33(-)CD38(-) fraction of umbilical cord CD34(+) cells. Exp. Hematol. 30:2002;582-589
51. Luens K.M., Travis M.A., Chen B.P., Hill B.L., Scollay R., Murray L.J. Thrombopoietin, kit ligand, and flk2/flt3 ligand together induce increased numbers of primitive hematopoietic progenitors from human CD34+Thy-1+Lin- cells with preserved ability to engraft SCID-hu bone. Blood. 91:1998;1206-1215
52. McKinstry W.J., Li C.L., Rasko J.E., Nicola N.A., Johnson G.R., Metcalf D. Cytokine receptor expression on hematopoietic stem and progenitor cells. Blood. 89:1997;65-71
53. McSweeney P.A., Rouleau K.A., Wallace P.M., Bruno B., Andrews R.G., Krizanac-Bengez L., Sandmaier B.M., Storb R., Wayner E., Nash R.A. Characterization of monoclonal antibodies that recognize canine CD34. Blood. 91:1998;1977-1986
54. Melniczek J.R., Dambach D., Prociuk U., Jezyk P.F., Henthorn P.S., Patterson D.F., Giger U. Sry-negative XX sex reversal in a family of Norwegian Elkhounds. J. Vet. Intern. Med. 13:1999;564-569
55. Miller C.L., Eaves C.J. Expansion in vitro of adult murine hematopoietic stem cells with transplantable lympho-myeloid reconstituting ability. Proc. Nat. Acad. Sci. USA. 94:1997;13648-13653
56. Morel F., Szilvassy S.J., Travis M., Chen B., Galy A. Primitive hematopoietic cells in murine bone marrow express the CD34 antigen. Blood. 88:1996;3774-3784
57. Morimoto M., Tsujimura T., Kanakura Y., Kitamura Y., Matsuda H. Expression of c-kit and stem cell factor mRNA in liver specimens from healthy adult dogs. Am. J. Vet. Res. 59:1998;363-366
58. Morrison S.J., Wandycz A.M., Hemmati H.D., Wright D.E., Weissman I.L. Identification of a lineage of multipotent hematopoietic progenitors. Development. 124:1997;1929-1939
59. + human fetal liver progenitors with a high proliferative potential. Blood. 83:1994;3170-3181
60. Muller A.M., Hermanns M.I., Skrzynski C., Nesslinger M., Muller K.M., Kirkpatrick C.J. Expression of the endothelial markers PECAM-1, vWf, and CD34 in vivo and in vitro. Exp. Mol. Pathol. 72:2002;221-229
61. Niemeyer G.P., Hudson J., Bredgman R., Spano J., Nash R.A., Lothrop C.D. Jr. Isolation and characterization of canine hematopoietic progenitor cells. Exp. Hematol. 29:2001;686-693
62. Noort W.A., Wilpshaar J., Hertogh C.D., Rad M., Lurvink E.G., van Luxemburg-Heijs S.A., Zwinderman K., Verwey R.A., Willemze R., Falkenburg J.H. Similar myeloid recovery despite superior overall engraftment in NOD/SCID mice after transplantation of human CD34(+) cells from umbilical cord blood as compared to adult sources. Bone Marrow Transpl. 28:2001;163-171
63. Ogawa M., Matsuzaki Y., Nishikawa S., Hayashi S., Kunisada T., Sudo T., Kina T., Nakauchi H. Expression and function of c-kit in hematopoietic progenitor cells. J. Exp. Med. 174:1991;63-71
64. Osawa M., Hanada K., Hamada H., Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 273:1996;242-245
65. Patterson D. Companion animal medicine in the age of medical genetics. J. Vet. Intern. Med. 14:2000;1-9
66. Pullen R.P., Somberg R.L., Felsburg P.J., Henthorn P.S. X-linked severe combined immunodeficiency in a family of Cardigan Welsh corgis. J. Am. Anim. Hosp. Assoc. 33:1997;494-499
67. +, rhodamine 123 (low) phenotype identifies a marrow cell population highly enriched for human hematopoietic stem cells. Leukemia. 12:1998;942-950
68. Rosler E.S., Brandt J.E., Chute J., Hoffman R. An in vivo competitive repopulation assay for various sources of human hematopoietic stem cells. Blood. 96:2000;3414-3421
69. + bone marrow cells. Blood. 84:1994;1473-1481
70. - cells: comparative study with stem cell factor or interleukin-3. Int. J. Hematol. 71:2000;33-39
71. Simmons P.J., Torok-Storb B. CD34 expression by stromal precursors in normal human adult bone marrow. Blood. 78:1991;2848-2853
72. Simmons P.J., Torok-Storb B. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody STRO-1. Blood. 78:1991;55-62
73. Sogo S., Inaba M., Ogata H., Hisha H., Adachi Y., Mori S., Toki J., Yamanishi K., Kanzaki H., Adachi M., Ikehara S. Induction of c-kit molecules on human CD34+/c-kit< low cells: evidence for CD34+/c-kit< low cells as primitive hematopoietic stem cells. Stem Cells. 15:1997;420-429
74. Somberg R.L., Pullen R.P., Casal M.L., Patterson D.F., Felsburg P.J., Henthorn P.S. A single nucleotide insertion in the canine interleukin-2 receptor gamma chain results in X-linked severe combined immunodeficiency disease. Vet. Immunol. Immunopathol. 47:1995;203-213
75. Somberg R.L., Robinson J.P., Felsburg P.J. T lymphocyte development and function in dogs with X-linked severe combined immunodeficiency. J. Immunol. 153:1994;4006-4015
76. Somberg R.L., Tipold A., Hartnett B.J., Moore P.F., Henthorn P.S., Felsburg P.J. Postnatal development of T cells in dogs with X-linked severe combined immunodeficiency. J. Immunol. 156:1996;1431-1435
77. Storb R., Yu C., Deeg H.J., Georges G., Kiem H.P., McSweeney P.A., Nash R.A., Sandmaier B.M., Sullivan K.M., Wagner J.L., Walters M.C. Current and future preparative regimens for bone marrow transplantation in thalassemia. Ann. NY Acad. Sci. 850:1998;276-287
78. Thilaganathan B., Nicolaides K.H., Morgan G. Subpopulations of CD34-positive haematopoietic progenitors in fetal blood. Br. J. Haematol. 87:1994;634-636
79. Turner C.W., Yeager A.M., Waller E.K., Wingard J.R., Fleming W.H. Engraftment potential of different sources of human hematopoietic progenitor cells in BNX mice. Blood. 87:1996;3237-3244
80. Wagner J.E., Broxmeyer H.E., Byrd R.L., Zehnbauer B., Schmeckpeper B., Shah N., Griffin C., Emanuel P.D., Zuckerman K.S., Cooper S., et al. Transplantation of umbilical cord blood after myeloablative therapy: analysis of engraftment. Blood. 79:1992;1874-1881. (see comments)
81. Wagner J.L., Burnett R.C., DeRose S.A., Francisco L.V., Storb R., Ostrander E.A. Histocompatibility testing of dog families with highly polymorphic microsatellite markers. Transplantation. 62:1996;876-877
82. + human hematopoietic progenitors from fetal liver, cord blood, and adult bone marrow respond differently to hematopoietic cytokines depending on the ontogenic source. Exp. Hematol. 26:1998;1034-1042
83. Wunderli P.S., Felsburg P.J. An improved method for the isolation of enriched canine peripheral blood mononuclear cell and peripheral blood lymphocyte preparations. Vet. Immunol. Immunopathol. 20:1989;335-344
84. Zandstra P.W., Conneally E., Piret J.M., Eaves C.J. Ontogeny-associated changes in the cytokine responses of primitive human haematopoietic cells. Br. J. Haematol. 101:1998;770-778