FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
American journal of veterinary research2017; 78(10); 1215-1228; doi: 10.2460/ajvr.78.10.1215

Effects of autologous stromal cells and cytokines on differentiation of equine bone marrow-derived progenitor cells.

Abstract: OBJECTIVE To develop an in vitro system for differentiation of equine B cells from bone marrow hematopoietic progenitor cells on the basis of protocols for other species. SAMPLE Bone marrow aspirates aseptically obtained from 12 research horses. PROCEDURES Equine bone marrow CD34 cells were sorted by use of magnetic beads and cultured in medium supplemented with cytokines (recombinant human interleukin-7, equine interleukin-7, stem cell factor, and Fms-like tyrosine kinase-3), murine OP9 stromal cell preconditioned medium, and equine fetal bone marrow mesenchymal stromal cell preconditioned medium. Cells in culture were characterized by use of flow cytometry, immunocytofluorescence microscopy, and quantitative reverse-transcriptase PCR assay. RESULTS For these culture conditions, bone marrow-derived equine CD34 cells differentiated into CD19IgM B cells that expressed the signature transcription factors early B-cell factor and transcription factor 3. These conditions also supported the concomitant development of autologous stromal cells, and their presence was supportive of B-cell development. CONCLUSIONS AND CLINICAL RELEVANCE Equine B cells were generated from bone marrow aspirates by use of supportive culture conditions. In vitro generation of equine autologous B cells should be of use in studies on regulation of cell differentiation and therapeutic transplantation.
Get Full Text
Publication Date: 2017-09-26 PubMed ID: 28945121PubMed Central: PMC5656228DOI: 10.2460/ajvr.78.10.1215Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research paper talks about the progress made in developing an in vitro system for differentiation of equine (horse) B cells from bone marrow hematopoietic progenitor cells. This was achieved by using certain supplementary components (cytokines and stromal cells), and the results showed successful creation of specific B cells. This process could be helpful in investigating cell differentiation regulation and therapeutic transplantation.

Objective

  • The research aimed to build an in vitro method where the B cells in horses can be differentiated from bone marrow hematopoietic progenitor cells. These methods are built based on protocols used for different species.

Sample

  • The researchers used bone marrow aspirates, which were aseptically obtained from 12 research horses.

Procedures

  • Sorted CD34 cells from equine bone marrow were cultured in a specialized medium, supplemented with certain cytokines (recombinant human interleukin-7, equine interleukin-7, stem cell factor, and Fms-like tyrosine kinase-3).
  • The conditioned medium from murine OP9 stromal cell and equine fetal bone marrow mesenchymal stromal cell was also added to these cultures.
  • Characterization of the cells in the culture was carried out with flow cytometry, immunocytofluorescence microscopy, and quantitative reverse-transcriptase PCR assay.

Results

  • The bone marrow-derived equine CD34 cells differentiated into CD19IgM B cells under the provided culture conditions. These B cells indicated the expression of signature transcription factors early B-cell factor and transcription factor 3.
  • The presence of autologous stromal cells was noticed alongside, and they were supportive of B-cell development.

Conclusions and Clinical Relevance

  • Equine B cells were successfully generated from bone marrow aspirates through the aid of supportive culture conditions.
  • The generation of these autologous B cells in lab conditions would be useful for studies related to regulation of cell differentiation and for therapeutic transplantation purposes.

Cite This Article

APA
Schwab UE, Tallmadge RL, Matychak MB, Felippe MJB. (2017). Effects of autologous stromal cells and cytokines on differentiation of equine bone marrow-derived progenitor cells. Am J Vet Res, 78(10), 1215-1228. https://doi.org/10.2460/ajvr.78.10.1215

Publication

American journal of veterinary research
ISSN: 1943-5681
NlmUniqueID: 0375011
Country: United States
Language: English
Volume: 78
Issue: 10
Pages: 1215-1228

Researcher Affiliations

Schwab, Ute E
    Tallmadge, Rebecca L
      Matychak, Mary Beth
        Felippe, M Julia B

          MeSH Terms

          • Animals
          • Bone Marrow Cells / cytology
          • Bone Marrow Cells / drug effects
          • Cell Differentiation
          • Cells, Cultured
          • Cytokines / pharmacology
          • Female
          • Flow Cytometry
          • Horses
          • Male
          • Mice
          • Stromal Cells / cytology

          Grant Funding

          • DP2 OD007216 / NIH HHS

          References

          This article includes 59 references
          1. Lin YC, Jhunjhunwala S, Benner C, Heinz S, Welinder E, Mansson R, Sigvardsson M, Hagman J, Espinoza CA, Dutkowski J, Ideker T, Glass CK, Murre C. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate.. Nat Immunol 2010 Jul;11(7):635-43.
            pmc: PMC2896911pubmed: 20543837doi: 10.1038/ni.1891google scholar: lookup
          2. Blom B, Spits H. Development of human lymphoid cells.. Annu Rev Immunol 2006;24:287-320.
            pubmed: 16551251doi: 10.1146/annurev.immunol.24.021605.090612google scholar: lookup
          3. LeBien TW, Tedder TF. B lymphocytes: how they develop and function.. Blood 2008 Sep 1;112(5):1570-80.
            pmc: PMC2518873pubmed: 18725575doi: 10.1182/blood-2008-02-078071google scholar: lookup
          4. Rawlings DJ, Quan SG, Kato RM, Witte ON. Long-term culture system for selective growth of human B-cell progenitors.. Proc Natl Acad Sci U S A 1995 Feb 28;92(5):1570-4.
            pmc: PMC42561pubmed: 7533295doi: 10.1073/pnas.92.5.1570google scholar: lookup
          5. Prieyl JA, LeBien TW. Interleukin 7 independent development of human B cells.. Proc Natl Acad Sci U S A 1996 Sep 17;93(19):10348-53.
            pmc: PMC38387pubmed: 8816803doi: 10.1073/pnas.93.19.10348google scholar: lookup
          6. Nishihara M, Wada Y, Ogami K, Ebihara Y, Ishii T, Tsuji K, Ueno H, Asano S, Nakahata T, Maekawa T. A combination of stem cell factor and granulocyte colony-stimulating factor enhances the growth of human progenitor B cells supported by murine stromal cell line MS-5.. Eur J Immunol 1998 Mar;28(3):855-64.
            pubmed: 9541580doi: 10.1002/(SICI)1521-4141(199803)28:03<855::AID-IMMU855>3.0.CO;2-Xgoogle scholar: lookup
          7. Barker J, Verfaillie CM. A novel in vitro model of early human adult B lymphopoiesis that allows proliferation of pro-B cells and differentiation to mature B lymphocytes.. Leukemia 2000 Sep;14(9):1614-20.
            pubmed: 10995008doi: 10.1038/sj.leu.2401869google scholar: lookup
          8. Ichii M, Oritani K, Yokota T, Schultz DC, Holter JL, Kanakura Y, Kincade PW. Stromal cell-free conditions favorable for human B lymphopoiesis in culture.. J Immunol Methods 2010 Jul 31;359(1-2):47-55.
            pmc: PMC2902975pubmed: 20540945doi: 10.1016/j.jim.2010.06.002google scholar: lookup
          9. Dorshkind K. In vitro differentiation of B lymphocytes from primitive hemopoietic precursors present in long-term bone marrow cultures.. J Immunol 1986 Jan;136(2):422-9.
            pubmed: 3484490
          10. Baird AM, Gerstein RM, Berg LJ. The role of cytokine receptor signaling in lymphocyte development.. Curr Opin Immunol 1999 Apr;11(2):157-66.
            pubmed: 10322150doi: 10.1016/s0952-7915(99)80027-2google scholar: lookup
          11. Tokoyoda K, Egawa T, Sugiyama T, Choi BI, Nagasawa T. Cellular niches controlling B lymphocyte behavior within bone marrow during development.. Immunity 2004 Jun;20(6):707-18.
            pubmed: 15189736doi: 10.1016/j.immuni.2004.05.001google scholar: lookup
          12. Nagasawa T. Microenvironmental niches in the bone marrow required for B-cell development.. Nat Rev Immunol 2006 Feb;6(2):107-16.
            pubmed: 16491135doi: 10.1038/nri1780google scholar: lookup
          13. Briquet A, Dubois S, Bekaert S, Dolhet M, Beguin Y, Gothot A. Prolonged ex vivo culture of human bone marrow mesenchymal stem cells influences their supportive activity toward NOD/SCID-repopulating cells and committed progenitor cells of B lymphoid and myeloid lineages.. Haematologica 2010 Jan;95(1):47-56.
            pmc: PMC2805732pubmed: 19713224doi: 10.3324/haematol.2009.008524google scholar: lookup
          14. Vieira P, Cumano A. Differentiation of B lymphocytes from hematopoietic stem cells.. Methods Mol Biol 2004;271:67-76.
            pubmed: 15146113doi: 10.1385/1-59259-796-3:067google scholar: lookup
          15. Cumano A, Dorshkind K, Gillis S, Paige CJ. The influence of S17 stromal cells and interleukin 7 on B cell development.. Eur J Immunol 1990 Oct;20(10):2183-9.
            pubmed: 2242755doi: 10.1002/eji.1830201006google scholar: lookup
          16. Rolink AG, ten Boekel E, Yamagami T, Ceredig R, Andersson J, Melchers F. B cell development in the mouse from early progenitors to mature B cells.. Immunol Lett 1999 May 3;68(1):89-93.
            pubmed: 10397161doi: 10.1016/s0165-2478(99)00035-8google scholar: lookup
          17. Billips LG, Petitte D, Dorshkind K, Narayanan R, Chiu CP, Landreth KS. Differential roles of stromal cells, interleukin-7, and kit-ligand in the regulation of B lymphopoiesis.. Blood 1992 Mar 1;79(5):1185-92.
            pubmed: 1371414
          18. Miller JP, Izon D, DeMuth W, Gerstein R, Bhandoola A, Allman D. The earliest step in B lineage differentiation from common lymphoid progenitors is critically dependent upon interleukin 7.. J Exp Med 2002 Sep 2;196(5):705-11.
            pmc: PMC2193997pubmed: 12208884doi: 10.1084/jem.20020784google scholar: lookup
          19. Kouro T, Yokota T, Welner R, Kincade PW. In vitro differentiation and measurement of B cell progenitor activity in culture.. Curr Protoc Immunol 2005 May;Chapter 22:Unit 22F.2.
            pubmed: 18432949doi: 10.1002/0471142735.im22f02s66google scholar: lookup
          20. Ray RJ, Paige CJ, Furlonger C, Lyman SD, Rottapel R. Flt3 ligand supports the differentiation of early B cell progenitors in the presence of interleukin-11 and interleukin-7.. Eur J Immunol 1996 Jul;26(7):1504-10.
            pubmed: 8766553doi: 10.1002/eji.1830260715google scholar: lookup
          21. Cho SK, Webber TD, Carlyle JR, Nakano T, Lewis SM, Zúñiga-Pflücker JC. Functional characterization of B lymphocytes generated in vitro from embryonic stem cells.. Proc Natl Acad Sci U S A 1999 Aug 17;96(17):9797-802.
            pmc: PMC22290pubmed: 10449774doi: 10.1073/pnas.96.17.9797google scholar: lookup
          22. Namikawa R, Muench MO, de Vries JE, Roncarolo MG. The FLK2/FLT3 ligand synergizes with interleukin-7 in promoting stromal-cell-independent expansion and differentiation of human fetal pro-B cells in vitro.. Blood 1996 Mar 1;87(5):1881-90.
            pubmed: 8634436
          23. Parekh C, Crooks GM. Critical differences in hematopoiesis and lymphoid development between humans and mice.. J Clin Immunol 2013 May;33(4):711-5.
            pmc: PMC3633618pubmed: 23274800doi: 10.1007/s10875-012-9844-3google scholar: lookup
          24. Espeli M, Rossi B, Mancini SJ, Roche P, Gauthier L, Schiff C. Initiation of pre-B cell receptor signaling: common and distinctive features in human and mouse.. Semin Immunol 2006 Feb;18(1):56-66.
            pubmed: 16337808doi: 10.1016/j.smim.2005.11.002google scholar: lookup
          25. Ghia P, ten Boekel E, Rolink AG, Melchers F. B-cell development: a comparison between mouse and man.. Immunol Today 1998 Oct;19(10):480-5.
            pubmed: 9785673doi: 10.1016/s0167-5699(98)01330-9google scholar: lookup
          26. Zhang Q, Iida R, Yokota T, Kincade PW. Early events in lymphopoiesis: an update.. Curr Opin Hematol 2013 Jul;20(4):265-72.
            pmc: PMC3676435pubmed: 23594693doi: 10.1097/MOH.0b013e3283612628google scholar: lookup
          27. Yoshikawa Y, Hirayama F, Kanai M, Nakajo S, Ohkawara J, Fujihara M, Yamaguchi M, Sato N, Kasai M, Sekiguchi S, Ikebuchi K. Stromal cell-independent differentiation of human cord blood CD34+CD38- lymphohematopoietic progenitors toward B cell lineage.. Leukemia 2000 Apr;14(4):727-34.
            pubmed: 10764162doi: 10.1038/sj.leu.2401713google scholar: lookup
          28. Kraus H, Kaiser S, Aumann K, Bönelt P, Salzer U, Vestweber D, Erlacher M, Kunze M, Burger M, Pieper K, Sic H, Rolink A, Eibel H, Rizzi M. A feeder-free differentiation system identifies autonomously proliferating B cell precursors in human bone marrow.. J Immunol 2014 Feb 1;192(3):1044-54.
            pubmed: 24379121doi: 10.4049/jimmunol.1301815google scholar: lookup
          29. Matsuo T. In vitro modulation of alkaline phosphatase activity in neutrophils from patients with chronic myelogenous leukemia by monocyte-derived activity.. Blood 1986 Feb;67(2):492-7.
            pubmed: 3484643
          30. Flaminio MJ, LaCombe V, Kohn CW, Antczak DF. Common variable immunodeficiency in a horse.. J Am Vet Med Assoc 2002 Nov 1;221(9):1296-302, 1267.
            pubmed: 12418696doi: 10.2460/javma.2002.221.1296google scholar: lookup
          31. Flaminio MJ, Tallmadge RL, Salles-Gomes CO, Matychak MB. Common variable immunodeficiency in horses is characterized by B cell depletion in primary and secondary lymphoid tissues.. J Clin Immunol 2009 Jan;29(1):107-16.
            pubmed: 18677444doi: 10.1007/s10875-008-9221-4google scholar: lookup
          32. Radcliffe CH, Flaminio MJ, Fortier LA. Temporal analysis of equine bone marrow aspirate during establishment of putative mesenchymal progenitor cell populations.. Stem Cells Dev 2010 Feb;19(2):269-82.
            pmc: PMC3138180pubmed: 19604071doi: 10.1089/scd.2009.0091google scholar: lookup
          33. Battista JM, Tallmadge RL, Stokol T, Felippe MJ. Hematopoiesis in the equine fetal liver suggests immune preparedness.. Immunogenetics 2014 Nov;66(11):635-49.
            pmc: PMC4198492pubmed: 25179685doi: 10.1007/s00251-014-0799-9google scholar: lookup
          34. Kraeft SK, Sutherland R, Gravelin L, Hu GH, Ferland LH, Richardson P, Elias A, Chen LB. Detection and analysis of cancer cells in blood and bone marrow using a rare event imaging system.. Clin Cancer Res 2000 Feb;6(2):434-42.
            pubmed: 10690521
          35. Fajardo-Orduña GR, Mayani H, Montesinos JJ. Hematopoietic Support Capacity of Mesenchymal Stem Cells: Biology and Clinical Potential.. Arch Med Res 2015 Nov;46(8):589-96.
            pubmed: 26522615doi: 10.1016/j.arcmed.2015.10.001google scholar: lookup
          36. Kydd J, Antczak DF, Allen WR, Barbis D, Butcher G, Davis W, Duffus WP, Edington N, Grünig G, Holmes MA. Report of the First International Workshop on Equine Leucocyte Antigens, Cambridge, UK, July 1991.. Vet Immunol Immunopathol 1994 Jul;42(1):3-60.
            pubmed: 7975180doi: 10.1016/0165-2427(94)90088-4google scholar: lookup
          37. Lunn DP, Holmes MA, Antczak DF, Agerwal N, Baker J, Bendali-Ahcene S, Blanchard-Channell M, Byrne KM, Cannizzo K, Davis W, Hamilton MJ, Hannant D, Kondo T, Kydd JH, Monier MC, Moore PF, O'Neil T, Schram BR, Sheoran A, Stott JL, Sugiura T, Vagnoni KE. Report of the Second Equine Leucocyte Antigen Workshop, Squaw valley, California, July 1995.. Vet Immunol Immunopathol 1998 Mar 31;62(2):101-43.
            pubmed: 9638857doi: 10.1016/s0165-2427(97)00160-8google scholar: lookup
          38. Saalmüller A, Lunney JK, Daubenberger C, Davis W, Fischer U, Göbel TW, Griebel P, Hollemweguer E, Lasco T, Meister R, Schuberth HJ, Sestak K, Sopp P, Steinbach F, Xiao-Wei W, Aasted B. Summary of the animal homologue section of HLDA8.. Cell Immunol 2005 Jul-Aug;236(1-2):51-8.
            pubmed: 16198325doi: 10.1016/j.cellimm.2005.08.009google scholar: lookup
          39. Steinbach F, Stark R, Ibrahim S, Gawad EA, Ludwig H, Walter J, Commandeur U, Mauel S. Molecular cloning and characterization of markers and cytokines for equid myeloid cells.. Vet Immunol Immunopathol 2005 Oct 18;108(1-2):227-36.
            pubmed: 16112744doi: 10.1016/j.vetimm.2005.07.015google scholar: lookup
          40. Kabithe E, Hillegas J, Stokol T, Moore J, Wagner B. Monoclonal antibodies to equine CD14.. Vet Immunol Immunopathol 2010 Nov 15;138(1-2):149-53.
            pubmed: 20674042doi: 10.1016/j.vetimm.2010.07.003google scholar: lookup
          41. Simmons PJ, Torok-Storb B. CD34 expression by stromal precursors in normal human adult bone marrow.. Blood 1991 Dec 1;78(11):2848-53.
            pubmed: 1720038
          42. Lin CS, Ning H, Lin G, Lue TF. Is CD34 truly a negative marker for mesenchymal stromal cells?. Cytotherapy 2012 Nov;14(10):1159-63.
            pmc: PMC3846603pubmed: 23066784doi: 10.3109/14653249.2012.729817google scholar: lookup
          43. Kurosaka D, LeBien TW, Pribyl JA. Comparative studies of different stromal cell microenvironments in support of human B-cell development.. Exp Hematol 1999 Aug;27(8):1271-81.
            pubmed: 10428504doi: 10.1016/s0301-472x(99)00067-3google scholar: lookup
          44. Taguchi T, Takenouchi H, Shiozawa Y, Matsui J, Kitamura N, Miyagawa Y, Katagiri YU, Takahashi T, Okita H, Fujimoto J, Kiyokawa N. Interleukin-7 contributes to human pro-B-cell development in a mouse stromal cell-dependent culture system.. Exp Hematol 2007 Sep;35(9):1398-407.
            pubmed: 17656007doi: 10.1016/j.exphem.2007.05.019google scholar: lookup
          45. Parrish YK, Baez I, Milford TA, Benitez A, Galloway N, Rogerio JW, Sahakian E, Kagoda M, Huang G, Hao QL, Sevilla Y, Barsky LW, Zielinska E, Price MA, Wall NR, Dovat S, Payne KJ. IL-7 Dependence in human B lymphopoiesis increases during progression of ontogeny from cord blood to bone marrow.. J Immunol 2009 Apr 1;182(7):4255-66.
            pmc: PMC2659466pubmed: 19299724doi: 10.4049/jimmunol.0800489google scholar: lookup
          46. Giebel B, Corbeil D, Beckmann J, Höhn J, Freund D, Giesen K, Fischer J, Kögler G, Wernet P. Segregation of lipid raft markers including CD133 in polarized human hematopoietic stem and progenitor cells.. Blood 2004 Oct 15;104(8):2332-8.
            pubmed: 15231568doi: 10.1182/blood-2004-02-0511google scholar: lookup
          47. Bender JG, Unverzagt KL, Walker DE, Lee W, Van Epps DE, Smith DH, Stewart CC, To LB. Identification and comparison of CD34-positive cells and their subpopulations from normal peripheral blood and bone marrow using multicolor flow cytometry.. Blood 1991 Jun 15;77(12):2591-6.
            pubmed: 1710512
          48. Walter K, Bonifer C, Tagoh H. Stem cell-specific epigenetic priming and B cell-specific transcriptional activation at the mouse Cd19 locus.. Blood 2008 Sep 1;112(5):1673-82.
            pubmed: 18552207doi: 10.1182/blood-2008-02-142786google scholar: lookup
          49. Weekx SF, Van Bockstaele DR, Plum J, Moulijn A, Rodrigus I, Lardon F, De Smedt M, Nijs G, Lenjou M, Loquet P, Berneman ZN, Snoeck HW. CD34++ CD38- and CD34+ CD38+ human hematopoietic progenitors from fetal liver, cord blood, and adult bone marrow respond differently to hematopoietic cytokines depending on the ontogenic source.. Exp Hematol 1998 Oct;26(11):1034-42.
            pubmed: 9766443
          50. Song K, Li L, Wang Y, Liu T. Hematopoietic stem cells: multiparameter regulation.. Hum Cell 2016 Apr;29(2):53-7.
            pubmed: 26883144doi: 10.1007/s13577-016-0134-xgoogle scholar: lookup
          51. Van Epps DE, Bender J, Lee W, Schilling M, Smith A, Smith S, Unverzagt K, Law P, Burgess J. Harvesting, characterization, and culture of CD34+ cells from human bone marrow, peripheral blood, and cord blood.. Blood Cells 1994;20(2-3):411-23.
            pubmed: 7538347
          52. Hao QL, Shah AJ, Thiemann FT, Smogorzewska EM, Crooks GM. A functional comparison of CD34 + CD38- cells in cord blood and bone marrow.. Blood 1995 Nov 15;86(10):3745-53.
            pubmed: 7579341
          53. Arakawa-Hoyt J, Dao MA, Thiemann F, Hao QL, Ertl DC, Weinberg KI, Crooks GM, Nolta JA. The number and generative capacity of human B lymphocyte progenitors, measured in vitro and in vivo, is higher in umbilical cord blood than in adult or pediatric bone marrow.. Bone Marrow Transplant 1999 Dec;24(11):1167-76.
            pubmed: 10642804doi: 10.1038/sj.bmt.1702048google scholar: lookup
          54. Voermans C, Gerritsen WR, von dem Borne AE, van der Schoot CE. Increased migration of cord blood-derived CD34+ cells, as compared to bone marrow and mobilized peripheral blood CD34+ cells across uncoated or fibronectin-coated filters.. Exp Hematol 1999 Dec;27(12):1806-14.
            pubmed: 10641598doi: 10.1016/s0301-472x(99)00113-7google scholar: lookup
          55. De Bruyn C, Delforge A, Lagneaux L, Bron D. Characterization of CD34+ subsets derived from bone marrow, umbilical cord blood and mobilized peripheral blood after stem cell factor and interleukin 3 stimulation.. Bone Marrow Transplant 2000 Feb;25(4):377-83.
            pubmed: 10723580doi: 10.1038/sj.bmt.1702145google scholar: lookup
          56. Rossi MI, Yokota T, Medina KL, Garrett KP, Comp PC, Schipul AH Jr, Kincade PW. B lymphopoiesis is active throughout human life, but there are developmental age-related changes.. Blood 2003 Jan 15;101(2):576-84.
            pubmed: 12393702doi: 10.1182/blood-2002-03-0896google scholar: lookup
          57. da Silva CL, Gonçalves R, Porada CD, Ascensão JL, Zanjani ED, Cabral JM, Almeida-Porada G. Differences amid bone marrow and cord blood hematopoietic stem/progenitor cell division kinetics.. J Cell Physiol 2009 Jul;220(1):102-11.
            pmc: PMC4008884pubmed: 19277981doi: 10.1002/jcp.21736google scholar: lookup
          58. Mold JE, Venkatasubrahmanyam S, Burt TD, Michaëlsson J, Rivera JM, Galkina SA, Weinberg K, Stoddart CA, McCune JM. Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans.. Science 2010 Dec 17;330(6011):1695-9.
            pmc: PMC3276679pubmed: 21164017doi: 10.1126/science.1196509google scholar: lookup
          59. Ekman A, Ilves M, Iivanainen A. B lymphopoiesis is characterized by pre-B cell marker gene expression in fetal cattle and declines in adults.. Dev Comp Immunol 2012 May;37(1):39-49.
            pubmed: 22210545doi: 10.1016/j.dci.2011.12.009google scholar: lookup

          Citations

          This article has been cited 0 times.
          Subscribe to our newsletter
          Join 99,727 horse owners like you who receive our email updates on horse health and nutrition.