The function of hematopoietic stem cells is altered by both genetic and inflammatory factors in lupus mice

Blood

Volumn 121, Issue 11, 2013, Pages 1986-1994

  Niu, Haitao ^a   Fang, Guoqiang ^a   Tang, Yiting ^a   Xie, Luokun ^a   Yang, Huan ^b   Morel, Laurence ^c   Diamond, Betty ^a   Zou, Yong Rui ^a,b  

^a North Shore LIJ Health System ^*  (United States)

^b FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2C; DOUBLE STRANDED DNA; GFI 1 PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN G; INTERFERON; INTERLEUKIN 10; INTERLEUKIN 6; MX1 PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN P18; PROTEIN P19; PROTEIN P21; PROTEIN P27; RNA POLYMERASE IIA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; AUTACOID; CDKN2C PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 1A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL LINEAGE; CLINICAL FEATURE; COMPARATIVE STUDY; CONTROLLED STUDY; GENE EXPRESSION; GENE LOCUS; GENETIC SUSCEPTIBILITY; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; STEM CELL MOBILIZATION; STEM CELL SELF-RENEWAL; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; CELL SURVIVAL; CONGENIC STRAIN; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MYELOPOIESIS; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL PROLIFERATION; CELL SURVIVAL; CYCLIN-DEPENDENT KINASE INHIBITOR P18; CYCLIN-DEPENDENT KINASE INHIBITOR P21; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELLS; INFLAMMATION MEDIATORS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MYELOPOIESIS; SIGNAL TRANSDUCTION;

MLCS; MLOWN;

EID: 84877619326     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-05-433755     Document Type: Article

References (55)

1. Cheshier SH, Morrison SJ, Liao X, et al. In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc Natl Acad Sci USA. 1999;96(6):3120-3125.
2. Wilson A, Laurenti E, Oser G, et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell. 2008;135(6):1118-1129.
3. Cheng T, Rodrigues N, Shen H, et al. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science. 2000;287(5459): 1804-1808.
4. Zon LI. Intrinsic and extrinsic control of haematopoietic stem-cell self-renewal. Nature. 2008;453(7193):306-313.
5. Li L, Xie T. Stem cell niche: Structure and function. Annu Rev Cell Dev Biol. 2005;21:605-631.
6. Randall TD, Weissman IL. Phenotypic and functional changes induced at the clonal level in hematopoietic stem cells after 5-fluorouracil treatment. Blood. 1997;89(10):3596-3606.
7. Cheshier SH, Prohaska SS, Weissman IL. The effect of bleeding on hematopoietic stem cell cycling and self-renewal. Stem Cells Dev. 2007; 16(5):707-717.
8. Rodriguez S, Chora A, Goumnerov B, et al. Dysfunctional expansion of hematopoietic stem cells and block of myeloid differentiation in lethal sepsis. Blood. 2009;114(19):4064-4076.
9. Scumpia PO, Kelly-Scumpia KM, Delano MJ, et al. Cutting edge: Bacterial infection induces hematopoietic stem and progenitor cell expansion in the absence of TLR signaling. J Immunol. 2010; 184(5):2247-2251.
10. Nagai Y, Garrett KP, Ohta S, et al. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity. 2006;24(6):801-812.
11. Ueda Y, Kondo M, Kelsoe G. Inflammation and the reciprocal production of granulocytes and lymphocytes in bone marrow. J Exp Med. 2005;201(11):1771-1780.
12. Esplin BL, Shimazu T, Welner RS, et al. Chronic exposure to a TLR ligand injures hematopoietic stem cells. J Immunol. 2011;186(9):5367-5375.
13. Kolb-Mäurer A, Weissinger F, Kurzai O, et al. Bacterial infection of human hematopoietic stem cells induces monocytic differentiation. FEMS Immunol Med Microbiol. 2004;40(2):147-153.
14. De Luca K, Frances-Duvert V, Asensio MJ, et al. The TLR1/2 agonist PAM(3)CSK(4) instructs commitment of human hematopoietic stem cells to a myeloid cell fate. Leukemia. 2009;23(11): 2063-2074.
15. Baldridge MT, King KY, Boles NC, et al. Quiescent haematopoietic stem cells are activated by IFN-gamma in response to chronic infection. Nature. 2010;465(7299):793-797.
16. Massberg S, Schaerli P, Knezevic-Maramica I, et al. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell. 2007;131(5): 994-1008.
17. Keeling DM, Isenberg DA. Haematological manifestations of systemic lupus erythematosus. Blood Rev. 1993;7(4):199-207.
18. Böhm I. Apoptosis: The link between autoantibodies and leuko-/lymphocytopenia in patients with lupus erythematosus. Scand J Rheumatol. 2004;33(6):409-416.
19. Rönnblom L, Alm GV, Eloranta ML. Type I interferon and lupus. Curr Opin Rheumatol. 2009; 21(5):471-477.
20. Banchereau J,PascualV.Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity. 2006;25(3):383-392
21. Aringer M, Smolen JS. The role of tumor necrosis factor-alpha in systemic lupus erythematosus. Arthritis Res Ther. 2008;10(1):202.
22. Rönnblom L, Elkon KB. Cytokines as therapeutic targets in SLE. Nat Rev Rheumatol. 2010;6(6): 339-347.
23. Blenman KR, Duan B, Xu Z, et al. IL-10 regulation of lupus in the NZM2410 murine model. Lab Invest. 2006;86(11):1136-1148.
24. Lacki JK, Samborski W, Mackiewicz SH. Interleukin-10 and interleukin-6 in lupus erythematosus and rheumatoid arthritis, correlations with acute phase proteins. Clin Rheumatol. 1997;16(3):275-278.
25. Maeda K, Malykhin A, Teague-Weber BN, et al. Interleukin-6 aborts lymphopoiesis and elevates production of myeloid cells in systemic lupus erythematosus-prone B6.Sle1.Yaa animals. Blood. 2009;113(19):4534-4540.
26. Essers MA, Offner S, Blanco-Bose WE, et al. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature. 2009;458(7240):904-908.
27. Kang YJ, Yang SJ, Park G, et al. A novel function of interleukin-10 promoting self-renewal of hematopoietic stem cells. Stem Cells. 2007;25(7): 1814-1822.
28. Pronk CJ, Veiby OP, Bryder D, et al. Tumor necrosis factor restricts hematopoietic stem cell activity in mice: Involvement of two distinct receptors. J Exp Med. 2011;208(8):1563-1570.
29. Chen C, Liu Y, Liu Y, et al. Mammalian target of rapamycin activation underlies HSC defects in autoimmune disease and inflammation in mice. J Clin Invest. 2010;120(11):4091-4101.
30. Morel L, Croker BP, Blenman KR, et al. Genetic reconstitution of systemic lupus erythematosus immunopathology with polycongenicmurine strains. Proc Natl Acad Sci USA. 2000;97(12):6670-6675.
31. Xu Z, Potula HH, Vallurupalli A, et al. Cyclindependent kinase inhibitor Cdkn2c regulates B cell homeostasis and function in the NZM2410- derived murine lupus susceptibility locus Sle2c1. J Immunol. 2011;186(12):6673-6682.
32. Zhang J, Grindley JC, Yin T, et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature. 2006;441(7092):518-522.
33. Yilmaz OH, Valdez R, Theisen BK, et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature. 2006; 441(7092):475-482.
34. Orford KW, Scadden DT. Deconstructing stem cell self-renewal: Genetic insights into cell-cycle regulation. Nat Rev Genet. 2008;9(2):115-128.
35. Hock H, Hamblen MJ, Rooke HM, et al. Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature. 2004;431(7011):1002-1007.
36. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature. 2003;423(6937):255-260.
37. Park IK, Qian D, Kiel M, et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 2003;423(6937):302-305.
38. Yuan Y, Shen H, Franklin DS, et al. In vivo selfrenewing divisions of haematopoietic stem cells are increased in the absence of the early G1-phase inhibitor, p18INK4C. Nat Cell Biol. 2004;6(5):436-442.
39. King KY, Goodell MA. Inflammatory modulation of HSCs: Viewing the HSC as a foundation for the immune response. Nat Rev Immunol. 2011; 11(10):685-692.
40. Takizawa H, Boettcher S, Manz MG. Demandadapted regulation of early hematopoiesis in infection and inflammation. Blood. 2012;119(13): 2991-3002.
41. Harrison DE, Astle CM. Loss of stem cell repopulating ability upon transplantation. Effects of donor age, cell number, and transplantation procedure. J Exp Med. 1982;156(6):1767-1779.
42. Dykstra B, Olthof S, Schreuder J, et al. Clonal analysis reveals multiple functional defects of aged murine hematopoietic stem cells. J Exp Med. 2011;208(13):2691-2703.
43. Beerman I, Bhattacharya D, Zandi S, et al. Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proc Natl Acad Sci USA. 2010;107(12):5465-5470.
44. Abdulahad DA, Westra J, Limburg PC, et al. HMGB1 in systemic lupus Erythematosus: Its role in cutaneous lesions development. Autoimmun Rev. 2010;9(10):661-665.
45. Zickert A, Palmblad K, Sundelin B, et al. Renal expression and serum levels of high mobility group box 1 protein in lupus nephritis. Arthritis Res Ther. 2012;14(1):R36.
46. Urbonaviciute V, Fürnrohr BG, Meister S, et al. Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: Implications for the pathogenesis of SLE. J Exp Med. 2008; 205(13):3007-3018.
47. Tyndall A. Cellular therapy of systemic lupus erythematosus. Lupus. 2009;18(5):387-393.
48. Harris HE, Andersson U, Pisetsky DS. HMGB1: A multifunctional alarmin driving autoimmune and inflammatory disease. Nat Rev Rheumatol. 2012; 8(4):195-202.
49. Shao WH, Cohen PL. Disturbances of apoptotic cell clearance in systemic lupus erythematosus. Arthritis Res Ther. 2011;13(1):202.
50. van Os R, Kamminga LM, Ausema A, et al. A Limited role for p21Cip1/Waf1 in maintaining normal hematopoietic stem cell functioning. Stem Cells. 2007;25(4):836-843.
51. Matsumoto A, Takeishi S, Kanie T, et al. p57 is required for quiescence and maintenance of adult hematopoietic stem cells. Cell Stem Cell. 2011; 9(3):262-271.
52. Zou P, Yoshihara H, Hosokawa K, et al. p57(Kip2) and p27(Kip1) cooperate to maintain hematopoietic stem cell quiescence through interactions with Hsc70. Cell Stem Cell. 2011;9(3):247-261.
53. LaBaer J, Garrett MD, Stevenson LF, et al. New functional activities for the p21 family of CDK inhibitors. Genes Dev. 1997;11(7):847-862.
54. Sherr CJ, Roberts JM. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev. 1999;13(12):1501-1512.
55. Fukuda S, Mantel CR, Pelus LM. Survivin regulates hematopoietic progenitor cell proliferation through p21WAF1/Cip1-dependent and -independent pathways. Blood. 2004;103(1):120-127.