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Hematopoiesis

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Tissue Functioning and Remodeling in the Circulatory and Ventilatory Systems

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Abstract

Hematopoietic cells, or hemopoietic cells, represent bone marrow-derived cell types that circulate in blood (including mature cell types and their precursors). Hematopoietic cells are categorized into myeloid cells (basophils, eosinophils, neutrophils, erythrocytes, thrombocytes, monocytes and macrophages, and mastocytes) and lymphoid cells (Blymphocytes, various types of Tlymphocytes, which are the only hematopoietic cells that can be generated elsewhere than in the bone marrow, and natural killer [NK] cells, that are cytotoxic lymphocytes also called large granular lymphocytes).

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Notes

  1. 1.

    αιματικo\(\varsigma \): associated with blood, πoιεo: to do.

  2. 2.

    Cell quiescence is associated with: (1) downregulation of cyclin-D1; (2) upregulation of cyclin-dependent kinase inhibitors CKI1a and CKI2a; (3) action of T-cell-intrinsic quiescence factor FoxO1; and (4) activation of P38MAPK [45]. Factor FoxO1 maintains cell quiescence and impedes T-cell activation by self-antigens, but does not prevent polyclonal T-cell activation. Polyclonal T cells diversify their activities, unlike antigen-specific T-cell clones, but generally remain restricted to certain antigens. On the other hand, polyclonal immunoglobulins (antibodies) are combination of immunoglobulins secreted against a specific antigen, each identifying a different antigen epitope (antigenic determinant) and generally obtained from different B-cell clones.

  3. 3.

    Allometric scaling can also be applied to basal metabolic rate, heart rate, arterial radii, etc. Most of the scaling powers \({\cdot }^{p}\) are multiples of 1/4. Computed power 3/4 can be related to a surface-to-volume ratio.

  4. 4.

    Membrane-bound stem cell factor, or cellular kinase in tyrosine (KIT or cKIT) ligand, after proteolytic cleavage, binds and activates SCFR receptor. Membrane-bound stem cell factor stimulates adhesion of hematopoietic stem and progenitor cells to stromal cells, because it activates integrins.

  5. 5.

    A lineage marker negative phenotype (Lin − ) corresponds, in mice, to CD2 − , CD3 − , CD4 − , CD5 − , CD8 − , CD161c − , PTPRc − , Ly76 − , Ly6g − . Hematopoietic stem cells can be precisely distinguished from other hematopoietic progenitors by the plasmalemmal expression of signaling lymphocytic activation molecules (SLAM), such as SLAMF1, SLAMF2, and SLAMF4 [48].

  6. 6.

    Marker VEGFR2 is also called fetal liver kinase FLK1 and kinase insert domain receptor (KDR). VEGFR2 + , cadherin-1 + precursors can differentiate into endothelial, primitive and definitive hematopoietic progenitor cells, cardiomyocytes, and mural cells.

  7. 7.

    At stage 1, a majority of cells is positive for the endothelial marker, angiopoietin-1 TIE2 receptor (a.k.a. Tyr endothelial kinase [TEK]), whereas a minority of cells is positive for α\(_{2\mathrm{B}}\) integrin (or CD41) that defines hematopoietic engagement. Afterward, the percentage of CD41 + cells rises and most cells are rapidly CD41 + , TIE2 − cells. Transient TIE2high, SCFR + cell population that contains both CD41 − and CD41 + cells hence represents a transitional population from which definitive hematopoietic progenitors originate.

  8. 8.

    The recombination-activating gene, or RING finger gene Rnf74, encodes enzymes that act in the rearrangement of immunoglobulin genes and T-cell receptors during VDJ recombination.

  9. 9.

    Two subpopulations of common lymphoid progenitors — CLP1 and CLP2 — coexist in the bone marrow and generate lymphocytes. Type-1 common lymphoid progenitors (CLP1 cells) are IL2Rα + (CD25), PTPRc − , SCFR − cells, whereas CLP2 cells are IL2Rα + , PTPRc + , SCFR − cells.

  10. 10.

    I.e., CD117high.

  11. 11.

    A.k.a. CD135, fetal liver kinase FLK2, and FMS-like Tyr kinase receptor FLT3.

  12. 12.

    Dendritic cells can have both lymphoid and myeloid origins, but have a developmental program that is independent from that of lymphoid and myeloid cells. Cells that can differentiate into dendritic cells often also have the potential to become B, T, and NK cells.

  13. 13.

    Extramedullary transient hematopoiesis, in the liver or spleen, occurs after bone marrow stress; but after repair, bone marrow hematopoiesis follows.

  14. 14.

    The endosteum is a bone remodeling site characterized by high concentrations of calcium ions. Extracellular Ca2 +  concentration is assessed by calcium-sensing receptors.

  15. 15.

    Chemokine CXCL12 can induce motility, chemotaxis, and adhesion of cells expressing its receptor, CXC-chemokine receptor-4, as well as secretion of matrix metalloproteinases and angiogenic factors, such as vascular endothelial growth factor. Association of CXCL12 and CXCR4 is required for retention and maintenance of adult hematopoietic stem cells.

  16. 16.

    Homing corresponds to recruitment of circulating hematopoietic stem cells to the bone marrow vasculature and subsequent extravasation that requires adhesion molecules, such as selectins and integrins. Small GTPases Rac1 and Rac2 are also implicated in homing and retention of hematopoietic stem cells in the endosteal bone marrow HSC niches.

  17. 17.

    The endosteal niche for hematopoietic stem cells is characterized by a high Ca2 +  concentration (more than 20-fold the plasmatic one), due to active bone remodeling in the endosteum by osteoclasts.

  18. 18.

    A.k.a. neutrophil gelatinase-associated lipocalin (NGAL) and migration-stimulating factor inhibitor (MSFI).

  19. 19.

    A.k.a. hematopoietic growth factor and steel factor (SLF).

  20. 20.

    Receptor Tyr kinases TIE1 and TIE2 are required in HSC maintainance in HSC microenvironment. Receptor TIE2 activated by angiopoietin-1 secreted by osteoblasts upregulates N-cadherin expression in hematopoietic stem cells and maintains HSC quiescence viaCKI1a cyclin-dependent kinase inhibitor.

  21. 21.

    CD34 + cells also comprise endothelial progenitor cells, vascular endothelial cells, T lymphocytes, mastocytes, and interstitial and dermic dendritic cells, as well as other tissue-specific stem cells, such as muscle satellite cells and epidermal precursors [65, 66].

  22. 22.

    Podocalyxin is also known as podocalyxin-like protein PodxL1 or PCLP1, thrombomucin, and GP135; and endoglycan as podocalyxin-like protein PodxL2 or PCLP2. Podocalyxin was originally identified as a marker of kidney glomerular epithelial cells (podocytes). Podocalyxin is also expressed on vascular endothelial cells and hematopoietic stem and progenitor cells [66]. Intracellular binding partners of members of the CD34 family include scaffolds sodium–hydrogen exchanger (NHE) regulatory factors (NHERF1–NHERF2), or solute carrier family SLC8a39 regulators (SLC8a39R1 and -R2), as well as adaptor CRK-like protein (CRKL) [66]. Both NHERF1 and NHERF2 possess a C-terminal ezrin–radixin–moesin (ERM)-binding site and 2 PDZ domains. Although CD34 does not interact with NHERF proteins in hematopoietic progenitor cells, it operates with CRKL adaptor.

  23. 23.

    A.k.a. bone sialoprotein BSP1, early T-lymphocyte activation ETA1, and secreted phosphoprotein SPP1.

  24. 24.

    A.k.a. hemopoietic gene protein and negative differentiation regulator (NDR).

  25. 25.

    A.k.a. friend of GATA protein FOG1, zinc finger domain-containing protein ZnF89a and ZnF408.

  26. 26.

    The family of MYC genes that encode subclass-E basic helix–loop–helix proteins encompasses: (1) cellular (MYC or CMYC [bHLHe39]); (2) small cell lung carcinoma-derived (LMYC [bHLHe38]); and (3) neuroblastoma-derived (NMYC [bHLHe37]) genes. The MYC gene has been discovered in patients with Burkitt lymphoma.

  27. 27.

    HOX genes are clustered on some chromosomes. In humans, 4 clusters exist (39 HOX genes each [68]): HOXA cluster in chromosome 7; HOXB cluster in chromosome 17; HOXC cluster in chromosome 12; and HOXD cluster in chromosome 2.

  28. 28.

    A.k.a. transcription factor E2α, E2A immunoglobulin enhancer-binding factor E12–E47, immunoglobulin transcription factor ITF1, and subclass-B basic helix–loop–helix protein bHLHb21.

  29. 29.

    A.k.a. immunoglobulin transcription factor ITF2, SL3-3 enhancer factor SEF2, E2-2, and bHLHb19.

  30. 30.

    A.k.a. human E-box-binding protein (HEB), human transcription factor HTF4, and bHLHb20.

  31. 31.

    Or E12.

  32. 32.

    Or E47.

  33. 33.

    Alternative transcription start sites in genes give rise to canonical (Can) and alternative (Alt) forms of TcF4 and TcF12 proteins. Proteins of the E2A set, TcFE2α and TcF3, as well as TcF4Can and TcF12Can, possess 2 activation domains AD1 and AD2, whereas TcF4Alt and TcF12Alt have a single activation domain [70]. Subtype TcF12Alt is highly expressed by CD4 − , CD8 − thymocytes.

  34. 34.

    Carboxy terminus of heat shock protein HSP70-interacting protein (CHIP) that promotes formation of a pre-ubiquitination complex including E3-ubiquitin ligase SKP1 (S-phase-kinase-associated protein)–cullin-1–F-box-protein complex SCFSKP2 binds E2A proteins.

  35. 35.

    T-cell acute lymphocytic leukemia protein-1, or stem cell leukemia factor (SCL), is involved in the generation of hematopoietic stem cells from mesoderm during embryongenesis. In adult mice, bHLHa17 is implicated in self-renewal of short-term repopulating hematopoietic stem cells and development of erythrocytes and megakaryocytes, but not for maintenance of long-term repopulating hematopoietic stem cells [70].

  36. 36.

    Lymphoblastic leukemia-derived sequence factor-1 heterodimerizes with E proteins to ensure self-renewal of long-term repopulating hematopoietic stem cells [70].

  37. 37.

    Homo- and heterodimeric E proteins bind to E-box sequence (preferentially CACCTG E-box sequence) of target genes and recruit transcriptional coactivators such as P300 and CBP histone acetyltransferases and RNA polymerase-2. Heterodimers composed of E proteins and class-2 bHLH factors associate with CATATG E-box sequence of target genes and recruit coactivators or corepressors, such as cyclin-D- and Runt-related transcription factor-1 translocated to protein-1 (Runx1T1), a.k.a. ETO corepressor (eight twenty one) and zinc finger MYND domain-containing protein ZMYND2, acute myeloid leukemia AML1 (Runx1)–ETO fusion protein, and Sin3a histone deacetylase complex subunit. The most frequent chromosomal translocation in acute leukemia creates the Runx1–Runx1T1 fusion protein, which represses transcription via Runx1 and immortalizes hematopoietic progenitor cells. On the other hand, heterodimers made up of E and ID proteins fail to activate gene transcription. E-box CANNTG (N denotes any nucleotide) sequences belong to the enhancer regions of genes that encode immunoglobulin heavy (IgH) and κ chain (Igκ) of immunoglobulin light (IgL) chain. In T lymphocytes, unlike B lymphocytes, E-box binding complexes contain high amounts of both bHLHb20 and bHLHb21 factors.

  38. 38.

    The lymphoid-primed multipotent progenitor pool is a subset of LIN − , SCFR + , SCA1 + cells that express STK1 kinase (or FMS-related Tyr kinase FLT3). They have the potential to develop into granulocytes, lymphocytes, and monocytes, but neither erythrocytes nor megakaryocytes.

  39. 39.

    Transcription factor bHLHa17 is coexpressed with stem cell factor receptor in hematopoietic progenitors. Factor bHLHa17 constitutes a nucleation factor for a multifactorial complex with LIM-only protein-2 (LMO2; a.k.a. rhombotin-like protein-1, rhombotin-2, and T-cell translocation protein TTG2), GATA1, GATA2, bHLHb21, and LIM domain-binding protein LDB1 (a.k.a. C-terminal LIM domain-binding protein CLIM2 and nuclear LIM interactor [NLI]) that specifically enhances SCFR promoter activity via Specificity protein SP1 [71]. It also forms heterodimers with bHLHb20 and bHLHb21 factors. Activation of the TAL1 gene is the most frequent gain-of-function mutation in T-cell acute lymphoblastic leukemia. Factor bHLHa17 acts as both an activator and repressor of transcription. The Sin3a–HDAC1 corepressor complex interacts with bHLHa17 to restrict its function in erythroid differentiation [72].

  40. 40.

    Runt-related transcription factor Runx1 is also termed Acute myeloid leukemia AML1.

  41. 41.

    Vascular regions that generate hematopoietic stem cell in mice comprise endothelia of the dorsal aorta and vitelline and umbilical arteries, as well as yolk sac blood islands and distal allantois and chorion that are precursors of the placenta. These independent sites constitute the conceptus.

  42. 42.

    Mechanical forces contribute to the regulation of the developing cardiovascular system in embryos. After initiation of the heartbeat, cells lining the dorsal aorta, placental vessels, and umbilical and vitelline arteries initiate expression of the transcription factor Runx1 [74].

  43. 43.

    Transcription factor SPI1 is also known as PU1 factor. This tissue-specific member of the ETS family of transcription factors is predominantly expressed in myeloid cells (granulocytes, monocytes, and macrophages) and B lymphocytes.

  44. 44.

    A.k.a. CCN3 and insulin-like growth factor-binding protein IGFBP9.

  45. 45.

    Trimer NFy is composed of NFyα, NFyβ, and NFyγ subunits encoded by the NFYA, NFYB, and NFYC genes.

  46. 46.

    Erythropoietin (Epo) and its receptor (EpoR) are also synthesized by neoplastic cells and tumor endothelial cells.

  47. 47.

    Different STAT5 isoforms are activated during the early and late differentiation stages of granulocytes. The transcription factors Signal transducers and activators of transcription (STAT) reside in a latent form in the cytoplasm and become phosphorylated by Janus kinases (JaK). Receptor gCSFR activates neither JaK1, JaK2, TyK2, STAT1, nor STAT3 in neutrophils upon gCSF stimulation [87].

  48. 48.

    A.k.a. heparin-binding brain mitogen (HBBM), heparin-binding growth factor HBGF8, neurite growth-promoting factor NEGF1, heparin affinity regulatory peptide (HARP), and heparin-binding growth-associated molecule (HBGAM).

  49. 49.

    When cells no longer replicate their DNA, endogenous double-stranded breaks that occur during DNA replication and compromise genomic integrity are strongly reduced or absent.

  50. 50.

    During double-stranded break repair, H2AX is phosphorylated by phosphatidylinositol 3-kinase. Phosphorylated H2AX then participates in DNA repair, replication, recombination and regulation of the cell cycle, as it binds various cell cycle and DNA-repair factors.

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  1. Project-team INRIA-UPMC-CNRS REO Laboratoire Jacques-Louis Lions, CNRS UMR 7598, Université Pierre et Marie Curie, Place Jussieu 4, 75252, Paris Cedex 05, France

    Marc Thiriet

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Thiriet, M. (2013). Hematopoiesis. In: Tissue Functioning and Remodeling in the Circulatory and Ventilatory Systems. Biomathematical and Biomechanical Modeling of the Circulatory and Ventilatory Systems, vol 5. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5966-8_2

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