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Transplanted spleen stromal cells with osteogenic potential support ectopic myelopoiesis


Autoři: Helen C. O’Neill aff001;  Hong K. Lim aff001;  Pravin Periasamy aff002;  Lavanya Kumarappan aff002;  Jonathan K. H. Tan aff001;  Terence J. O’Neill aff004
Působiště autorů: Clem Jones Research Centre for Regenerative Medicine, Bond University, Gold Coast, Queensland, Australia aff001;  Research School of Biology, Australian National University, Canberra, Australian Capital Territory, Australia aff002;  Department of Microbiology, Yoo Long School of Medicine, National University of Singapore, Singapore, Singapore aff003;  Big Data Centre, Bond Business School, Bond University, Gold Coast, Queensland, Australia aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223416

Souhrn

Spleen stromal lines which support in vitro hematopoiesis are investigated for their lineage origin and hematopoietic support function in vivo. Marker expression and gene profiling identify a lineage relationship with mesenchymal stem cells and perivascular reticular cells described recently in bone marrow. Stromal lines commonly express Cxcl12, Pdgfra and Pdgfr typical of bone marrow derived perivascular reticular cells but reflect a unique cell type in terms of other gene and marker expression. Their classification as osteoprogenitors is confirmed through ability to undergo osteogenic, but not adipogenic or chondrogenic differentiation. Some stromal lines were shown to form ectopic niches for HSCs following engraftment under the kidney capsule of NOD/SCID mice. The presence of myeloid cells and a higher representation of a specific dendritic-like cell type over other myeloid cells within grafts was consistent with previous in vitro evidence of hematopoietic support capacity. These studies reinforce the role of perivascular/perisinusoidal reticular cells in hematopoiesis and implicate such cells as niches for hematopoiesis in spleen.

Klíčová slova:

Cell differentiation – Cell staining – Flow cytometry – Gene expression – Spleen – Stromal cells – Bone marrow cells – Hematopoiesis


Zdroje

1. Wolber FM, Leonard E, Michael S, Orschell-Traycoff CM, Yoder MC, Srour EF. Roles of spleen and liver in development of the murine hematopoietic system. Experimental Hematology. 2002;30(9):1010–9. doi: 10.1016/s0301-472x(02)00881-0 12225792

2. Tan JK, O'Neill HC. Myelopoiesis in spleen-producing distinct dendritic-like cells. Journal of Cellular and Molecular Medicine. 2012;16(8):1924–33. Epub 2011/11/29. doi: 10.1111/j.1582-4934.2011.01490.x 22117595.

3. Morita Y, Iseki A, Okamura S, Suzuki S, Nakauchi H, Ema H. Functional characterization of hematopoietic stem cells in the spleen. Experimental Hematology. 2011;39(3):351–9. doi: 10.1016/j.exphem.2010.12.008 21185906

4. Dor FJ, Ramirez ML, Parmar K, Altman EL, Huang CA, Down JD, et al. Primitive hematopoietic cell populations reside in the spleen: Studies in the pig, baboon, and human. Experimental Hematology. 2006;34(11):1573–82. Epub 2006/10/19. doi: 10.1016/j.exphem.2006.06.016 17046577.

5. Massberg S, Schaerli P, Knezevic-Maramica I, Köllnberger M, Tubo N, Moseman EA, et al. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell. 2007;131(5):994–1008. doi: 10.1016/j.cell.2007.09.047 18045540

6. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121(7):1109–21. doi: 10.1016/j.cell.2005.05.026 15989959.

7. Inra CN, Zhou BO, Acar M, Murphy MM, Richardson J, Zhao Z, et al. A perisinusoidal niche for extramedullary haematopoiesis in the spleen. Nature. 2015;527(7579):466–71. doi: 10.1038/nature15530 26570997; PubMed Central PMCID: PMC4838203.

8. Oda A, Tezuka T, Ueno Y, Hosoda S, Amemiya Y, Notsu C, et al. Niche-induced extramedullary hematopoiesis in the spleen is regulated by the transcription factor Tlx1. Sci Rep. 2018;8(1):8308. Epub 2018/05/29. doi: 10.1038/s41598-018-26693-x 29844356; PubMed Central PMCID: PMC5974313.

9. Hey YY, O'Neill HC. Antigen presenting properties of a myeloid dendritic-like cell in murine spleen. PLOS ONE. 2016;11(9):e0162358. Epub 2016/09/23. doi: 10.1371/journal.pone.0162358 27654936; PubMed Central PMCID: PMC5031434.

10. Hey YY, Tan JKH, O'Neill HC. Redefining Myeloid Cell Subsets in Murine Spleen. Front Immunol. 2016;6(652). doi: 10.3389/fimmu.2015.00652 26793192

11. Petvises S, Talaulikar D, O'Neill HC. Delineation of a novel dendritic-like subset in human spleen. Cellular & Molecular Immunology. 2016;13(4):443–50. Epub 2015/04/22. doi: 10.1038/cmi.2015.16 25891217; PubMed Central PMCID: PMC4947811.

12. O'Neill HC, Wilson HL, Quah B, Abbey JL, Despars G, Ni K. Dendritic cell development in long-term spleen stromal cultures. Stem Cells. 2004;22(4):475–86. Epub 2004/07/28. doi: 10.1634/stemcells.22-4-475 15277694.

13. Petvises S, O'Neill HC. Distinct progenitor origin distinguishes a lineage of dendritic-like cells in spleen. Frontiers in Immunology. 2014;4:501. Epub 2014/01/16. doi: 10.3389/fimmu.2013.00501 24427160; PubMed Central PMCID: PMC3877830.

14. O'Neill HC, Griffiths KL, Periasamy P, Hinton RA, Hey YY, Tan JKH. Spleen as a Site for Hematopoiesis of a Distinct Antigen Presenting Cell Type. Stem Cells International. 2011;2011. doi: 10.4061/2011/954275 22190965

15. Wilson HL, Ni K, O'Neill HC. Identification of progenitor cells in long-term spleen stromal cultures that produce immature dendritic cells. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(9):4784–9. Epub 2000/04/12. doi: 10.1073/pnas.080278897 10758164; PubMed Central PMCID: PMC18310.

16. Wilson HL, O'Neill HC. Identification of differentially expressed genes representing dendritic cell precursors and their progeny. Blood. 2003;102(5):1661–9. Epub 2003/05/17. doi: 10.1182/blood-2002-08-2426 12750154.

17. O'Neill HC, Griffiths KL, Periasamy P, Hinton RA, Petvises S, Hey YY, et al. Spleen stroma maintains progenitors and supports long-term hematopoiesis. Current stem cell research & therapy. 2014;9(4):354–63. Epub 2014/04/22. 24745998.

18. Despars G O'Neill HC. Splenic endothelial cell lines support development of dendritic cells from bone marrow. Stem cells. 2006;24(6):1496–504. Epub 2006/06/14. doi: 10.1634/stemcells.2005-0530 16769761.

19. Periasamy P, Tan JKH, Griffiths KL, O' Neill HC. Splenic stromal niches support hematopoiesis of dendritic-like cells from precursors in bone marrow and spleen. Experimental Hematology. 2009;37(9):1060–71. doi: 10.1016/j.exphem.2009.06.001 19539692

20. Ni K, O'Neill H. Spleen stromal cells support haemopoiesis and in vitro growth of dendritic cells from bone marrow. British Journal of Haematology. 1999;105(1):58–67. 10233363

21. Despars G, O'Neill HC. Heterogeneity amongst splenic stromal cell lines which support dendritic cell hematopoiesis. In vitro cellular & developmental biology Animal. 2006;42(7):208–15. Epub 2006/09/05. doi: 10.1290/0602016.1 16948502.

22. Hinton RA, O'Neill HC. Technical advance: in vitro production of distinct dendritic-like antigen-presenting cells from self-renewing hematopoietic stem cells. J Leukoc Biol. 2012;91(2):341–6. Epub 2011/11/15. doi: 10.1189/jlb.0611302 22075929.

23. Periasamy P, O'Neill HC. Stroma-dependent development of two dendritic-like cell types with distinct antigen presenting capability. Experimental Hematology. 2013;41(3):281–92. https://doi.org/10.1016/j.exphem.2012.11.003 23178375

24. Petvises S, O'Neill HC. Characterisation of dendritic cells arising from progenitors endogenous to murine spleen. PloS one. 2014;9(2):e88311. doi: 10.1371/journal.pone.0088311 24551086; PubMed Central PMCID: PMC3925139.

25. Periasamy P, Tan JKH, Griffiths KL, O'Neill HC. Splenic stromal niches support hematopoiesis of dendritic-like cells from precursors in bone marrow and spleen. Experimental Hematology. 2009;37(9):1060–71. doi: 10.1016/j.exphem.2009.06.001 19539692

26. Periasamy P, Petvises S, O'Neill HC. Development of two distinct dendritic-like APCs in the context of splenic stroma. Front Immunol. 2013;4:73. Epub 2013/03/23. doi: 10.3389/fimmu.2013.00073 23519558; PubMed Central PMCID: PMC3602895.

27. Petvises S, O'Neill HC. Distinct progenitor origin distinguishes a lineage of dendritic-like cells in spleen. Front Immunol. 2014;4:501. doi: 10.3389/fimmu.2013.00501 24427160; PubMed Central PMCID: PMC3877830.

28. Periasamy P, Petvises S, O'Neill HC. Development of two distinct dendritic-like APCs in the context of splenic stroma. Frontiers of Immunology. 2013;4:73. Epub 2013/03/23. doi: 10.3389/fimmu.2013.00073 23519558; PubMed Central PMCID: PMC3602895.

29. Corselli M, Chin CJ, Parekh C, Sahaghian A, Wang W, Ge S, et al. Perivascular support of human hematopoietic stem/progenitor cells. Blood. 2013;121(15):2891–901. Epub 2013/02/16. doi: 10.1182/blood-2012-08-451864 23412095; PubMed Central PMCID: PMC3707421.

30. Despars G, Periasamy P, Tan J, Abbey J, O'Neill TJ, O'Neill HC. Gene signature of stromal cells which support dendritic cell development. Stem cells and development. 2008;17(5):917–27. Epub 2008/06/20. doi: 10.1089/scd.2007.0170 18564035.

31. Tan JK, Periasamy P, O'Neill HC. Delineation of precursors in murine spleen that develop in contact with splenic endothelium to give novel dendritic-like cells. Blood. 2010;115(18):3678–85. Epub 2010/03/06. doi: 10.1182/blood-2009-06-227108 20203267.

32. Nadri S, Soleimani M, Hosseni RH, Massumi M, Atashi A, Izadpanah R. An efficient method for isolation of murine bone marrow mesenchymal stem cells. Int J Dev Biol. 2007;51(8):723–9. Epub 2007/10/17. doi: 10.1387/ijdb.072352ns 17939119.

33. Eslaminejad MB, Nikmahzar A, Taghiyar L, Nadri S, Massumi M. Murine mesenchymal stem cells isolated by low density primary culture system. Dev Growth Differ. 2006;48(6):361–70. Epub 2006/07/29. doi: 10.1111/j.1440-169X.2006.00874.x 16872449.

34. Stanford CM, Jacobson PA, Eanes ED, Lembke LA, Midura RJ. Rapidly forming apatitic mineral in an osteoblastic cell line (UMR 106–01 BSP). J Biol Chem. 1995;270(16):9420–8. Epub 1995/04/21. doi: 10.1074/jbc.270.16.9420 7721867.

35. Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, Pittenger MF. Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng. 1998;4(4):415–28. Epub 1999/01/23. doi: 10.1089/ten.1998.4.415 9916173.

36. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284. doi: 10.1126/science.284.5411.143 10102814

37. Qian SW, Li X, Zhang YY, Huang HY, Liu Y, Tang QQ. Characterisation of adipocyte differentiation from human mesenchymal stem cells in bone marrow. BMC Developmental Biology. 2010;10:47. doi: 10.1186/1471-213X-10-47 20459638

38. Petvises S, Periasamy P, O'Neill HC. MCSF drives regulatory DC development in stromal co-cultures supporting hematopoiesis. BMC Immunol. 2018;19(1):21. Epub 2018/06/26. doi: 10.1186/s12865-018-0255-y 29940852; PubMed Central PMCID: PMC6020213.

39. Periasamy P, Tan JK, O'Neill HC. Novel splenic antigen-presenting cells derive from a Lin(-) c-kit(lo) progenitor. Journal of Leukocyte Biology. 2013;93(1):63–9. Epub 2012/10/27. doi: 10.1189/jlb.0512260 23099325.

40. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–7. Epub 2006/08/23. doi: 10.1080/14653240600855905 16923606.

41. Halfon S, Abramov N, Grinblat B, Ginis I. Markers distinguishing mesenchymal stem cells from fibroblasts are downregulated with passaging. Stem Cells Dev. 2011;20(1):53–66. Epub 2010/10/26. doi: 10.1089/scd.2010.0040 20528146.

42. Morikawa S, Mabuchi Y, Kubota Y, Nagai Y, Niibe K, Hiratsu E, et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med. 2009;206(11):2483–96. Epub 2009/10/19. doi: 10.1084/jem.20091046 19841085; PubMed Central PMCID: PMC2768869.

43. Schieker M, Pautke C, Haasters F, Schieker J, Docheva D, Böcker W, et al. Human mesenchymal stem cells at the single-cell level: simultaneous seven-colour immunofluorescence. J Anat. 2007;210(5):592–9. doi: 10.1111/j.1469-7580.2007.00716.x 17451534; PubMed Central PMCID: PMC2375738.

44. Omatsu Y, Sugiyama T, Kohara H, Kondoh G, Fujii N, Kohno K, et al. The Essential Functions of Adipo-osteogenic Progenitors as the Hematopoietic Stem and Progenitor Cell Niche. Immunity. 2010;33(3):387–99. doi: 10.1016/j.immuni.2010.08.017 20850355

45. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 2006;25(6):977–88. doi: 10.1016/j.immuni.2006.10.016 17174120.

46. Kiel MJ, Morrison SJ. Maintaining Hematopoietic Stem Cells in the Vascular Niche. Immunity. 2006;25(6):862–4. doi: 10.1016/j.immuni.2006.11.005 17174928

47. Ehninger A, Trumpp A. The bone marrow stem cell niche grows up: mesenchymal stem cells and macrophages move in. J Exp Med. 2011;208(3):421–8. doi: 10.1084/jem.20110132 21402747; PubMed Central PMCID: PMC3058583.

48. Oh I-H, Kwon K-R. Concise Review: Multiple Niches for Hematopoietic Stem Cell Regulations. STEM CELLS. 2010;28(7):1243–9. doi: 10.1002/stem.453 20517982

49. Pinho S, Lacombe J, Hanoun M, Mizoguchi T, Bruns I, Kunisaki Y, et al. PDGFRα and CD51 mark human nestin+ sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion. J Exp Med. 2013;210(7):1351–67. Epub 2013/06/17. doi: 10.1084/jem.20122252 23776077; PubMed Central PMCID: PMC3698522.

50. Nagasawa T, Omatsu Y, Sugiyama T. Control of hematopoietic stem cells by the bone marrow stromal niche: the role of reticular cells. Trends in Immunology. 2011;32(7):315–20. doi: 10.1016/j.it.2011.03.009 21531624

51. Mueller SN, Germain RN. Stromal cell contributions to the homeostasis and functionality of the immune system. Nature Reviews Immunology. 2009;9(9):618–29. http://www.nature.com/nri/journal/v9/n9/suppinfo/nri2588_S1.html 19644499

52. Wanjare M, Kusuma S, Gerecht S. Defining Differences among Perivascular Cells Derived from Human Pluripotent Stem Cells. Stem Cell Reports. 2014;2(5):746. Epub 2014/05/06. doi: 10.1016/j.stemcr.2014.04.012 28081437; PubMed Central PMCID: PMC4050475.

53. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3(3):301–13. doi: 10.1016/j.stem.2008.07.003 18786417

54. Farnsworth RH, Achen MG, Stacker SA. Lymphatic endothelium: an important interactive surface for malignant cells. Pulm Pharmacol Ther. 2006;19(1):51–60. Epub 2005/11/16. doi: 10.1016/j.pupt.2005.02.003 16286238.

55. Asada N, Takeishi S, Frenette PS. Complexity of bone marrow hematopoietic stem cell niche. Int J Hematol. 2017;106(1):45–54. Epub 2017/05/22. doi: 10.1007/s12185-017-2262-9 28534115.

56. Lv FJ, Tuan RS, Cheung KM, Leung VY. Concise review: the surface markers and identity of human mesenchymal stem cells. Stem Cells. 2014;32(6):1408–19. doi: 10.1002/stem.1681 24578244.

57. da Silva Meirelles L, Malta TM, de Deus Wagatsuma VM, Palma PV, Araújo AG, Ribeiro Malmegrim KC, et al. Cultured Human Adipose Tissue Pericytes and Mesenchymal Stromal Cells Display a Very Similar Gene Expression Profile. Stem Cells Dev. 2015;24(23):2822–40. Epub 2015/08/19. doi: 10.1089/scd.2015.0153 26192741; PubMed Central PMCID: PMC4653823.

58. Sidney LE, Branch MJ, Dunphy SE, Dua HS, Hopkinson A. Concise review: evidence for CD34 as a common marker for diverse progenitors. Stem Cells. 2014;32(6):1380–9. doi: 10.1002/stem.1661 24497003; PubMed Central PMCID: PMC4260088.

59. Crisan M, Corselli M, Chen WC, Peault B. Perivascular cells for regenerative medicine. J Cell Mol Med. 2012;16(12):2851–60. Epub 2012/08/14. doi: 10.1111/j.1582-4934.2012.01617.x 22882758; PubMed Central PMCID: PMC4393715.

60. Tasev D, Konijnenberg LS, Amado-Azevedo J, van Wijhe MH, Koolwijk P, van Hinsbergh VW. CD34 expression modulates tube-forming capacity and barrier properties of peripheral blood-derived endothelial colony-forming cells (ECFCs). Angiogenesis. 2016;19(3):325–38. Epub 2016/04/05. doi: 10.1007/s10456-016-9506-9 27043316; PubMed Central PMCID: PMC4930476.

61. Wilting J, Papoutsi M, Christ B, Nicolaides KH, von Kaisenberg CS, Borges J, et al. The transcription factor Prox1 is a marker for lymphatic endothelial cells in normal and diseased human tissues. Faseb J. 2002;16(10):1271–3. Epub 2002/06/13. doi: 10.1096/fj.01-1010fje 12060670.

62. Calloni R, Cordero EA, Henriques JA, Bonatto D. Reviewing and updating the major molecular markers for stem cells. Stem Cells Dev. 2013;22(9):1455–76. Epub 2013/01/22. doi: 10.1089/scd.2012.0637 23336433; PubMed Central PMCID: PMC3629778.

63. Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature. 2012;481(7382):457–62. Epub 2012/01/28. doi: 10.1038/nature10783 22281595; PubMed Central PMCID: PMC3270376.

64. Castagnaro L, Lenti E, Maruzzelli S, Spinardi L, Migliori E, Farinello D, et al. Nkx2-5(+)islet1(+) mesenchymal precursors generate distinct spleen stromal cell subsets and participate in restoring stromal network integrity. Immunity. 2013;38(4):782–91. doi: 10.1016/j.immuni.2012.12.005 23601687; PubMed Central PMCID: PMC3652017.

65. Asada N, Kunisaki Y, Pierce H, Wang Z, Fernandez NF, Birbrair A, et al. Differential cytokine contributions of perivascular haematopoietic stem cell niches. Nat Cell Biol. 2017;19(3):214–23. Epub 2017/02/20. doi: 10.1038/ncb3475 28218906; PubMed Central PMCID: PMC5467892.

66. Bouamar H, Zhang Y, Jouni D, Wittner M, Bensidhoum M, Jarrier P, et al. CXCR7 expression restricts CXCR4/SDF-1 mediated hematopoieitic-supporting activity of stromal cells by decreasing extracellular SDF-1 availability. Blood. 2009;114.

67. Allan EH, Ho PW, Umezawa A, Hata J, Makishima F, Gillespie MT, et al. Differentiation potential of a mouse bone marrow stromal cell line. J Cell Biochem. 2003;90(1):158–69. Epub 2003/08/26. doi: 10.1002/jcb.10614 12938165.

68. Tropel P, Noel D, Platet N, Legrand P, Benabid AL, Berger F. Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow. Exp Cell Res. 2004;295(2):395–406. Epub 2004/04/20. doi: 10.1016/j.yexcr.2003.12.030 15093739.

69. Aubin JE. Bone stem cells. J Cell Biochem Suppl. 1998;30–31:73–82. Epub 1999/01/20. 9893258.

70. Papathanasiou P, Attema JL, Karsunky H, Xu J, Smale ST, Weissman IL. Evaluation of the long-term reconstituting subset of hematopoietic stem cells with CD150. Stem Cells. 2009;27(10):2498–508. doi: 10.1002/stem.170 19593793; PubMed Central PMCID: PMC2783507.

71. Kunisaki Y, Bruns I, Scheiermann C, Ahmed J, Pinho S, Zhang D, et al. Arteriolar niches maintain haematopoietic stem cell quiescence. Nature. 2013;502(7473):637–43. doi: 10.1038/nature12612 24107994; PubMed Central PMCID: PMC3821873.

72. Greenbaum A, Hsu YM, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN, et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature. 2013;495(7440):227–30. Epub 2013/02/26. doi: 10.1038/nature11926 23434756; PubMed Central PMCID: PMC3600148.

73. Hughes CS, Postovit LM, Lajoie GA. Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics. 2010;10(9):1886–90. Epub 2010/02/18. doi: 10.1002/pmic.200900758 20162561.

74. Kleinman HK, McGarvey ML, Liotta LA, Robey PG, Tryggvason K, Martin GR. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry. 1982;21(24):6188–93. Epub 1982/11/23. doi: 10.1021/bi00267a025 6217835.

75. Orkin RW, Gehron P, McGoodwin EB, Martin GR, Valentine T, Swarm R. A murine tumor producing a matrix of basement membrane. The Journal of Experimental Medicine. 1977;145(1):204–20. Epub 1977/01/01. doi: 10.1084/jem.145.1.204 830788; PubMed Central PMCID: PMC2180589.

76. Tan JK, Watanabe T. Murine spleen tissue regeneration from neonatal spleen capsule requires lymphotoxin priming of stromal cells. Journal of immunology (Baltimore, Md: 1950). 2014;193(3):1194–203. Epub 2014/06/22. doi: 10.4049/jimmunol.1302115 24951816; PubMed Central PMCID: PMC4105237.

77. Tan JK, Watanabe T. Stromal Cell Subsets Directing Neonatal Spleen Regeneration. Sci Rep. 2017;7:40401. Epub 2017/01/09. doi: 10.1038/srep40401 28067323; PubMed Central PMCID: PMC5220291.

78. Tan JK, Quah BJ, Griffiths KL, Periasamy P, Hey YY, O'Neill HC. Identification of a novel antigen cross-presenting cell type in spleen. Journal of Cellular and Molecular Medicine. 2011;15(5):1189–99. Epub 2010/05/19. doi: 10.1111/j.1582-4934.2010.01089.x 20477902.

79. Sandberg ML, Sutton SE, Pletcher MT, Wiltshire T, Tarantino LM, Hogenesch JB, et al. c-Myb and p300 regulate hematopoietic stem cell proliferation and differentiation. Dev Cell. 2005;8(2):153–66. doi: 10.1016/j.devcel.2004.12.015 15691758.

80. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 2012;336(6077):86–90. Epub 2012/03/22. doi: 10.1126/science.1219179 22442384.

81. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci. 2007;10(12):1538–43. Epub 2007/11/18. doi: 10.1038/nn2014 18026097.

82. Merad M, Manz MG, Karsunky H, Wagers A, Peters W, Charo I, et al. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat Immunol. 2002;3(12):1135–41. Epub 2002/11/04. doi: 10.1038/ni852 12415265; PubMed Central PMCID: PMC4727838.

83. Hey YY, Quah B, O'Neill HC. Antigen presenting capacity of murine splenic myeloid cells. BMC Immunol. 2017;18(1):4. Epub 2017/01/11. doi: 10.1186/s12865-016-0186-4 28077081; PubMed Central PMCID: PMC5225582.

84. Tan JKH, Watanabe T. Determinants of postnatal spleen tissue regeneration and organogenesis. NPJ Regen Med. 2018;3:1. Epub 2018/01/26. doi: 10.1038/s41536-018-0039-2 29367882; PubMed Central PMCID: PMC5770394.


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