Identification of factors promoting ex vivo maintenance of mouse hematopoietic stem cells by long-term single-cell quantification

Blood

Volumn 128, Issue 9, 2016, Pages 1181-1192

  Kokkaliaris, Konstantinos D ^a,b   Drew, Erin ^a   Endele, Max ^a,b   Loeffler, Dirk ^a,b   Hoppe, Philipp S ^a,b   Hilsenbeck, Oliver ^a,b   Schauberger, Bernhard ^a   Hinzen, Christoph ^a   Skylaki, Stavroula ^a,b   Theodorou, Marina ^a   Kieslinger, Matthias ^a   Lemischka, Ihor ^c   Moore, Kateri ^c   Schroeder, Timm ^a,b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b ETH ZURICH   (Switzerland)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DERMATOPONTIN; SCLEROPROTEIN; UNCLASSIFIED DRUG; DPT PROTEIN, MOUSE; PROTEOCHONDROITIN SULFATE;

AFT024 STROMA CELL LINE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ADHESION; CELL DEATH; CELL DIVISION; CELL FATE; CELL FUNCTION; CELL ISOLATION; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CELL TRACKING; CLONOGENESIS; COCULTURE; CONTROLLED STUDY; ECTOPIC EXPRESSION; EX VIVO STUDY; EXTRACELLULAR MATRIX; GENE EXPRESSION; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE CELL ANALYSIS; STEM CELL CULTURE; STEM CELL SELF-RENEWAL; STROMA CELL; ANIMAL; CELL CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECTS; GENETICS; MALE; METABOLISM; TIME FACTOR; TRANSGENIC MOUSE;

ANIMALS; CELL CULTURE TECHNIQUES; CELL LINE; CELL SURVIVAL; CHONDROITIN SULFATE PROTEOGLYCANS; EXTRACELLULAR MATRIX PROTEINS; HEMATOPOIETIC STEM CELLS; MALE; MICE; MICE, TRANSGENIC; STROMAL CELLS; TIME FACTORS;

EID: 85016325794     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-03-705590     Document Type: Article

References (92)

1. Thomas ED, Lochte HL Jr, Lu WC, Ferrebee JW. Intravenous infusion of bone marrow in patients receiving radiation and chemotherapy. N Engl J Med. 1957;257(11):491-496.
2. Tyndall A, Gratwohl A. Blood and marrow stem cell transplants in autoimmune disease. A consensus report written on behalf of the European League Against Rheumatism (EULAR) and the European Group for Blood and Marrow Transplantation (EBMT). Br J Rheumatol. 1997;36(3):390-392.
3. Shizuru JA, Negrin RS, Weissman IL. Hematopoietic stem and progenitor cells: clinical and preclinical regeneration of the hematolymphoid system. Annu Rev Med. 2005;56:509-538.
4. Anisimov SV. Cell therapy for Parkinson's disease: II. Somatic stem cell-based applications [in Russian]. Adv Gerontol. 2009;22(1):150-166.
5. Takizawa H, Schanz U, Manz MG. Ex vivo expansion of hematopoietic stem cells: mission accomplished? Swiss Med Wkly. 2011;141:w13316.
6. Bodine DM, Karlsson S, Nienhuis AW. Combination of interleukins 3 and 6 preserves stem cell function in culture and enhances retrovirus-mediated gene transfer into hematopoietic stem cells. Proc Natl Acad Sci USA. 1989;86(22):8897-8901.
7. Ku H, Yonemura Y, Kaushansky K, Ogawa M. Thrombopoietin, the ligand for the Mpl receptor, synergizes with steel factor and other early acting cytokines in supporting proliferation of primitive hematopoietic progenitors of mice. Blood. 1996; 87(11):4544-4551.
8. Miller CL, Eaves CJ. Expansion in vitro of adult murine hematopoietic stem cells with transplantable lympho-myeloid reconstituting ability. Proc Natl Acad Sci USA. 1997;94(25):13648-13653.
9. Matsunaga T, Kato T, Miyazaki H, Ogawa M. Thrombopoietin promotes the survival of murine hematopoietic long-term reconstituting cells: comparison with the effects of FLT3/FLK-2 ligand and interleukin-6. Blood. 1998;92(2):452-461.
10. Ema H, Takano H, Sudo K, Nakauchi H. In vitro self-renewal division of hematopoietic stem cells. J Exp Med. 2000;192(9):1281-1288.
11. Himburg HA, Muramoto GG, Daher P, et al. Pleiotrophin regulates the expansion and regeneration of hematopoietic stem cells. Nat Med. 2010;16(4):475-482.
12. Zhang CC, Lodish HF. Insulin-like growth factor 2 expressed in a novel fetal liver cell population is a growth factor for hematopoietic stem cells. Blood. 2004;103(7):2513-2521.
13. de Haan G, Weersing E, Dontje B, et al. In vitro generation of long-term repopulating hematopoietic stem cells by fibroblast growth factor-1. Dev Cell. 2003;4(2):241-251.
14. Zhang CC, Kaba M, Ge G, et al. Angiopoietin-like proteins stimulate ex vivo expansion of hematopoietic stem cells. Nat Med. 2006;12(2):240-245.
15. Sauvageau G, Iscove NN, Humphries RK. In vitro and in vivo expansion of hematopoietic stem cells. Oncogene. 2004;23(43):7223-7232.
16. Walasek MA, van Os R, de Haan G. Hematopoietic stem cell expansion: challenges and opportunities. Ann N Y Acad Sci. 2012;1266:138-150.
17. Nakauchi H, Sudo K, Ema H. Quantitative assessment of the stem cell self-renewal capacity. Ann N Y Acad Sci. 2001;938:18-25.
18. Uchida N, Dykstra B, Lyons KJ, Leung FYK, Eaves CJ. Different in vivo repopulating activities of purified hematopoietic stem cells before and after being stimulated to divide in vitro with the same kinetics. Exp Hematol. 2003;31(12):1338-1347.
19. Metcalf D. Hematopoietic cytokines. Blood. 2008; 111(2):485-491.
20. Kamminga LM, Bystrykh LV, de Boer A, et al. The Polycomb group gene Ezh2 prevents hematopoietic stem cell exhaustion. Blood. 2006; 107(5):2170-2179.
21. Antonchuk J, Sauvageau G, Humphries RK. HOXB4-induced expansion of adult hematopoietic stem cells ex vivo. Cell. 2002;109(1):39-45.
22. Ohta H, Sekulovic S, Bakovic S, et al. Nearmaximal expansions of hematopoietic stem cells in culture using NUP98-HOX fusions. Exp Hematol. 2007;35(5):817-830.
23. Fischbach NA, Rozenfeld S, Shen W, et al. HOXB6 overexpression in murine bone marrow immortalizes a myelomonocytic precursor in vitro and causes hematopoietic stem cell expansion and acute myeloid leukemia in vivo. Blood. 2005; 105(4):1456-1466.
24. Boitano AE, Wang J, Romeo R, et al. Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science. 2010;329(5997):1345-1348.
25. Fares I, Chagraoui J, Gareau Y, et al. Cord blood expansion. Pyrimidoindole derivatives are agonists of human hematopoietic stem cell selfrenewal. Science. 2014;345(6203):1509-1512.
26. Baum C, von Kalle C, Staal FJ, et al. Chance or necessity? Insertional mutagenesis in gene therapy and its consequences. Mol Ther. 2004;9(1):5-13.
27. Zhang XB, Beard BC, Trobridge GD, et al. High incidence of leukemia in large animals after stem cell gene therapy with a HOXB4-expressing retroviral vector. J Clin Invest. 2008;118(4): 1502-1510.
28. Krosl J, Austin P, Beslu N, Kroon E, Humphries RK, Sauvageau G. In vitro expansion of hematopoietic stem cells by recombinant TATHOXB4 protein. Nat Med. 2003;9(11):1428-1432.
29. Moore KA, Ema H, Lemischka IR. In vitro maintenance of highly purified, transplantable hematopoietic stem cells. Blood. 1997;89(12): 4337-4347.
30. Oostendorp RA, Harvey KN, Kusadasi N, et al. Stromal cell lines from mouse aorta-gonadsmesonephros subregions are potent supporters of hematopoietic stem cell activity. Blood. 2002;99(4): 1183-1189.
31. Thiemann FT, Moore KA, Smogorzewska EM, Lemischka IR, Crooks GM. The murine stromal cell line AFT024 acts specifically on human CD34+CD38-progenitors to maintain primitive function and immunophenotype in vitro. Exp Hematol. 1998;26(7):612-619.
32. Punzel M, Moore KA, Lemischka IR, Verfaillie CM. The type of stromal feeder used in limiting dilution assays influences frequency and maintenance assessment of human long-term culture initiating cells. Leukemia. 1999;13(1):92-97.
33. Lewis ID, Almeida-Porada G, Du J, et al. Umbilical cord blood cells capable of engrafting in primary, secondary, and tertiary xenogeneic hosts are preserved after ex vivo culture in a noncontact system. Blood. 2001;97(11):3441-3449.
34. Nolta JA, Thiemann FT, Arakawa-Hoyt J, et al. The AFT024 stromal cell line supports long-term ex vivo maintenance of engrafting multipotent human hematopoietic progenitors. Leukemia. 2002;16(3):352-361.
35. Punzel M, Gupta P, Verfaillie CM. The microenvironment of AFT024 cells maintains primitive human hematopoiesis by counteracting contact mediated inhibition of proliferation. Cell Commun Adhes. 2002;9(3):149-159.
36. Hutton JF, Rozenkov V, Khor FSL, D'Andrea RJ, Lewis ID. Bone morphogenetic protein 4 contributes to the maintenance of primitive cord blood hematopoietic progenitors in an ex vivo stroma-noncontact co-culture system. Stem Cells Dev. 2006;15(6):805-813.
37. Muller-Sieburg CE, Cho RH, Karlsson L, Huang JF, Sieburg HB. Myeloid-biased hematopoietic stem cells have extensive self-renewal capacity but generate diminished lymphoid progeny with impaired IL-7 responsiveness. Blood. 2004; 103(11):4111-4118.
38. Sieburg HB, Cho RH, Dykstra B, Uchida N, Eaves CJ, Muller-Sieburg CE. The hematopoietic stem compartment consists of a limited number of discrete stem cell subsets. Blood. 2006;107(6):2311-2316.
39. Dykstra B, Kent D, Bowie M, et al. Long-term propagation of distinct hematopoietic differentiation programs in vivo. Cell Stem Cell. 2007;1(2):218-229.
40. Kent DG, Copley MR, Benz C, et al. Prospective isolation and molecular characterization of hematopoietic stem cells with durable self-renewal potential. Blood. 2009;113(25):6342-6350.
41. Punzel M, Liu D, Zhang T, Eckstein V, Miesala K, Ho AD. The symmetry of initial divisions of human hematopoietic progenitors is altered only by the cellular microenvironment. Exp Hematol. 2003; 31(4):339-347.
42. Kent DG, Dykstra BJ, Cheyne J, Ma E, Eaves CJ. Steel factor coordinately regulates the molecular signature and biologic function of hematopoietic stem cells. Blood. 2008;112(3):560-567.
43. Sekulovic S, Gasparetto M, Lecault V, et al. Ontogeny stage-independent and high-level clonal expansion in vitro of mouse hematopoietic stem cells stimulated by an engineered NUP98-HOX fusion transcription factor. Blood. 2011;118(16):4366-4376.
44. Hackney JA, Charbord P, Brunk BP, Stoeckert CJ, Lemischka IR, Moore KA. A molecular profile of a hematopoietic stem cell niche. Proc Natl Acad Sci USA. 2002;99(20):13061-13066.
45. Charbord P, Moore K. Gene expression in stem cell-supporting stromal cell lines. Ann N Y Acad Sci. 2005;1044:159-167.
46. Hadjantonakis A-K, Macmaster S, Nagy A. Embryonic stem cells and mice expressing different GFP variants for multiple non-invasive reporter usage within a single animal. BMC Biotechnol. 2002;2:11.
47. Wineman J, Moore K, Lemischka I, Müller-Sieburg C. Functional heterogeneity of the hematopoietic microenvironment: rare stromal elements maintain long-term repopulating stem cells. Blood. 1996;87(10):4082-4090.
48. Eilken HM, Nishikawa S, Schroeder T. Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature. 2009;457(7231):896-900.
49. Rieger MA, Hoppe PS, Smejkal BM, Eitelhuber AC, Schroeder T. Hematopoietic cytokines can instruct lineage choice. Science. 2009;325(5937):217-218.
50. 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.
51. 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):1109-1121.
52. Schroeder T. Long-term single-cell imaging of mammalian stem cells. Nat Methods. 2011; 8(suppl 4):S30-S35.
53. Kokkaliaris KD, Loeffler D, Schroeder T. Advances in tracking hematopoiesis at the single-cell level. Curr Opin Hematol. 2012;19(4):243-249.
54. Endele M, Schroeder T. Molecular live cell bioimaging in stem cell research. Ann N Y Acad Sci. 2012;1266:18-27.
55. Coutu DL, Schroeder T. Probing cellular processes by long-term live imaging-historic problems and current solutions. J Cell Sci. 2013; 126(Pt 17):3805-3815.
56. Wohrer S, Knapp DJHF, Copley MR, et al. Distinct stromal cell factor combinations can separately control hematopoietic stem cell survival, proliferation, and self-renewal. Cell Reports. 2014;7(6):1956-1967.
57. Lutolf MP, Doyonnas R, Havenstrite K, Koleckar K, Blau HM. Perturbation of single hematopoietic stem cell fates in artificial niches. Integr Biol (Camb). 2009;1(1):59-69.
58. Dykstra B, Ramunas J, Kent D, et al. Highresolution video monitoring of hematopoietic stem cells cultured in single-cell arrays identifies new features of self-renewal. Proc Natl Acad Sci USA. 2006;103(21):8185-8190.
59. Benveniste P, Frelin C, Janmohamed S, et al. Intermediate-term hematopoietic stem cells with extended but time-limited reconstitution potential. Cell Stem Cell. 2010;6(1):48-58.
60. Buckley SM, Ulloa-Montoya F, Abts D, et al. Maintenance of HSC by Wnt5a secreting AGMderived stromal cell line. Exp Hematol. 2011; 39(1):114-123.e1-5.
61. Oostendorp RAJ, Robin C, Steinhoff C, et al. Long-term maintenance of hematopoietic stem cells does not require contact with embryoderived stromal cells in cocultures. Stem Cells. 2005;23(6):842-851.
62. Falix FA, Aronson DC, Lamers WH, Gaemers IC. Possible roles of DLK1 in the Notch pathway during development and disease. Biochim Biophys Acta. 2012;1822(6):988-995.
63. Smas CM, Chen L, Sul HS. Cleavage of membrane-associated pref-1 generates a soluble inhibitor of adipocyte differentiation. Mol Cell Biol. 1997;17(2):977-988.
64. Garcés C, Ruiz-Hidalgo MJ, Bonvini E, Goldstein J, Laborda J. Adipocyte differentiation is modulated by secreted delta-like (dlk) variants and requires the expression of membrane-associated dlk. Differentiation. 1999;64(2):103-114.
65. Raghunandan R, Ruiz-Hidalgo M, Jia Y, et al. Dlk1 influences differentiation and function of B lymphocytes. Stem Cells Dev. 2008;17(3): 495-507.
66. Baladrón V, Ruiz-Hidalgo MJ, Nueda ML, et al. dlk acts as a negative regulator of Notch1 activation through interactions with specific EGF-like repeats. Exp Cell Res. 2005;303(2):343-359.
67. Radtke F, Wilson A, Stark G, et al. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity. 1999;10(5):547-558.
68. Kim KA, Kim JH, Wang Y, Sul HS. Pref-1 (preadipocyte factor 1) activates the MEK/extracellular signal-regulated kinase pathway to inhibit adipocyte differentiation. Mol Cell Biol. 2007;27(6):2294-2308.
69. Miyaoka Y, Tanaka M, Imamura T, Takada S, Miyajima A. A novel regulatory mechanism for Fgf18 signaling involving cysteine-rich FGF receptor (Cfr) and delta-like protein (Dlk). Development. 2010;137(1):159-167.
70. Moore KA, Pytowski B, Witte L, Hicklin D, Lemischka IR. Hematopoietic activity of a stromal cell transmembrane protein containing epidermal growth factor-like repeat motifs. Proc Natl Acad Sci USA. 1997;94(8):4011-4016.
71. Chou S, Lodish HF. Fetal liver hepatic progenitors are supportive stromal cells for hematopoietic stem cells. Proc Natl Acad Sci USA. 2010; 107(17):7799-7804.
72. Chou S, Flygare J, Lodish HF. Fetal hepatic progenitors support long-term expansion of hematopoietic stem cells. Exp Hematol. 2013; 41(5):479-490.e4.
73. Mirshekar-Syahkal B, Haak E, Kimber GM, et al. Dlk1 is a negative regulator of emerging hematopoietic stem and progenitor cells. Haematologica. 2013;98(2):163-171.
74. Niedermeyer J, Enenkel B, Park JE, et al. Mouse fibroblast-activation protein-conserved Fap gene organization and biochemical function as a serine protease. Eur J Biochem. 1998;254(3):650-654.
75. Lee KN, Jackson KW, Christiansen VJ, Lee CS, Chun JG, McKee PA. Antiplasmin-cleaving enzyme is a soluble form of fibroblast activation protein. Blood. 2006;107(4):1397-1404.
76. Jacob M, Chang L, Puré E. Fibroblast activation protein in remodeling tissues. Curr Mol Med. 2012;12(10):1220-1243.
77. Cheng JD, Valianou M, Canutescu AA, et al. Abrogation of fibroblast activation protein enzymatic activity attenuates tumor growth. Mol Cancer Ther. 2005;4(3):351-360.
78. Niedermeyer J, Kriz M, Hilberg F, et al. Targeted disruption of mouse fibroblast activation protein. Mol Cell Biol. 2000;20(3):1089-1094.
79. Roberts EW, Deonarine A, Jones JO, et al. Depletion of stromal cells expressing fibroblast activation protein-α from skeletal muscle and bone marrow results in cachexia and anemia. J Exp Med. 2013;210(6):1137-1151.
80. Superti-Furga A, Rocchi M, Schäfer BW, Gitzelmann R. Complementary DNA sequence and chromosomal mapping of a human proteoglycan-binding cell-adhesion protein (dermatopontin). Genomics. 1993;17(2):463-467.
81. Forbes EG, Cronshaw AD, MacBeath JR, Hulmes DJ. Tyrosine-rich acidic matrix protein (TRAMP) is a tyrosine-sulphated and widely distributed protein of the extracellular matrix. FEBS Lett. 1994;351(3):433-436.
82. Takeda U, Utani A, Wu J, et al. Targeted disruption of dermatopontin causes abnormal collagen fibrillogenesis. J Invest Dermatol. 2002; 119(3):678-683.
83. Leyte A, van Schijndel HB, Niehrs C, et al. Sulfation of Tyr1680 of human blood coagulation factor VIII is essential for the interaction of factor VIII with von Willebrand factor. J Biol Chem. 1991; 266(2):740-746.
84. Okamoto O, Fujiwara S, Abe M, Sato Y. Dermatopontin interacts with transforming growth factor beta and enhances its biological activity. Biochem J. 1999;337(Pt 3):537-541.
85. Okamoto O, Fujiwara S. Dermatopontin, a novel player in the biology of the extracellular matrix. Connect Tissue Res. 2006;47(4):177-189.
86. Yamazaki S, Ema H, Karlsson G, et al. Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell. 2011;147(5):1146-1158.
87. Yamazaki S, Iwama A, Takayanagi S, Eto K, Ema H, Nakauchi H. TGF-β as a candidate bone marrow niche signal to induce hematopoietic stem cell hibernation. Blood. 2009;113(6):1250-1256.
88. Larsson J, Blank U, Helgadottir H, et al. TGF-beta signaling-deficient hematopoietic stem cells have normal self-renewal and regenerative ability in vivo despite increased proliferative capacity in vitro. Blood. 2003;102(9):3129-3135.
89. Williams DA, Rios M, Stephens C, Patel VP. Fibronectin and VLA-4 in haematopoietic stem cell-microenvironment interactions. Nature. 1991; 352(6334):438-441.
90. Forsberg EC, Smith-Berdan S. Parsing the niche code: the molecular mechanisms governing hematopoietic stem cell adhesion and differentiation. Haematologica. 2009;94(11):1477-1481.
91. Schreiber TD, Steinl C, Essl M, et al. The integrin alpha9beta1 on hematopoietic stem and progenitor cells: involvement in cell adhesion, proliferation and differentiation. Haematologica. 2009;94(11):1493-1501.
92. Nilsson SK, Johnston HM, Whitty GA, et al. Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood. 2005;106(4):1232-1239.