Identification of in vitro HSC fate regulators by differential lipid raft clustering

Cell Cycle

Volumn 11, Issue 8, 2012, Pages 1535-1543

  Vannini, Nicola ^a   Roch, Aline ^a   Naveiras, Olaia ^a,b   Griffa, Alessandra ^a   Kobel, Stefan ^a   Lutolf, Matthias P ^a  

^a EPFL   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Hematopoietic stem cells; Hydrogel; Lipid rafts; Microwell array; Niche

Indexed keywords

INTERLEUKIN 3; INTERLEUKIN 6; OSTEOPONTIN; STEM CELL FACTOR; VASCULOTROPIN; WNT3A PROTEIN; WNT5A PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE PROGRESSION; CELLULAR DISTRIBUTION; CLUSTER ANALYSIS; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; LIPID RAFT; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; SIGNAL TRANSDUCTION;

EID: 84860338812     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.19900     Document Type: Article

References (56)

1. Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008; 132:598-611; PMID:18295578; http://dx.doi.org/10.1016/j.cell.2008.01.038.
2. Orford KW, Scadden DT. Deconstructing stem cell self-renewal: genetic insights into cell cycle regulation. Nat Rev Genet 2008; 9:115-28; PMID:18202695; http://dx.doi.org/10.1038/nrg2269.
3. Hills M, Lücke K, Chavez EA, Eaves CJ, Lansdorp PM. Probing the mitotic history and developmental stage of hematopoietic cells using single telomere length analysis (STELA). Blood 2009; 113:5765-75; PMID:19359409; http://dx.doi.org/10.1182/blood-2009-01-198374.
4. Cheng T, Rodrigues N, Shen H, Yang Y, Dombkowski D, Sykes M, et al. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 2000; 287:1804-8; PMID:10710306; http://dx.doi.org/10.1126/science.287.5459.1804.
5. Passegué E, Wagers AJ, Giuriato S, Anderson WC, Weissman IL. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J Exp Med 2005; 202:1599-611; PMID:16330818; http://dx.doi.org/10.1084/jem.20050967.
6. Trumpp A, Essers M, Wilson A. Awakening dormant haematopoietic stem cells. Nat Rev Immunol 2010; 10:201-9; PMID:20182459; http://dx.doi.org/10.1038/ nri2726.
7. Mantel C, Broxmeyer HE. Sirtuin 1, stem cells, aging and stem cell aging. Curr Opin Hematol 2008; 15:326-31; PMID:18536570; http://dx.doi.org/10.1097/ MOH.0b013e3283043819.
8. Fortunel NO, Hatzfeld A, Hatzfeld JA. Transforming growth factor-beta: pleiotropic role in the regulation of hematopoiesis. Blood 2000; 96:2022-36.9
9. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004; 118:149-61; PMID:15260986; http://dx.doi.org/10.1016/j.cell.2004.07.004.
10. Arai F, Yoshihara H, Hosokawa K, Nakamura Y, Gomei Y, Iwasaki H, et al. Niche regulation of hematopoietic stem cells in the endosteum. Ann NY Acad Sci 2009; 1176:36-46; PMID:19796231; http://dx.doi.org/10.1111/j.1749-6632.2009. 04561.x.
11. Nemeth MJ, Topol L, Anderson SM, Yang Y, Bodine DM. Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. Proc Natl Acad Sci USA 2007; 104:15436-41; PMID:17881570; http://dx.doi.org/10. 1073/pnas.0704747104.
12. 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; 25:977-88; PMID:17174120; http://dx.doi.org/10.1016/j.immuni.2006.10.016.
13. Stier S, Ko Y, Forkert R, Lutz C, Neuhaus T, Grünewald E, et al. Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med 2005; 201:1781-91; PMID:15928197; http://dx.doi.org/10.1084/jem.20041992.
14. Nilsson SK, Johnston HM, Whitty GA, Williams B, Webb RJ, Denhardt DT, et al. Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 2005; 106:1232-9; PMID:15845900; http://dx.doi.org/10.1182/blood-2004-11-4422.
15. Grassinger J, Haylock DN, Storan MJ, Haines GO, Williams B, Whitty GA, et al. Thrombin-cleaved osteopontin regulates hemopoietic stem and progenitor cell functions through interactions with alpha9beta1 and alpha4beta1 integrins. Blood 2009; 114:49-59; PMID:19417209; http://dx.doi.org/10.1182/blood-2009-01- 197988.
16. Zhang J, Grindley JC, Yin T, Jayasinghe S, He XC, Ross JT, et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 2006; 441:518-22; PMID:16633340; http://dx.doi.org/10.1038/ nature04747.
17. Yamazaki S, Iwama A, Morita Y, Eto K, Ema H, Nakauchi H. Cytokine signaling, lipid raft clustering and HSC hibernation. Ann NY Acad Sci 2007; 1106:54-63; PMID:17442772; http://dx.doi.org/10.1196/annals.1392.017.
18. Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, et al. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 2009; 458:904-8; PMID:19212321; http://dx.doi.org/10.1038/nature07815.
19. Chen C, Liu Y, Liu Y, Zheng P. The axis of mTOR-mitochondria-ROS and stemness of the hematopoietic stem cells. Cell Cycle 2009; 8:1158-60; PMID:19270502; http://dx.doi.org/10.4161/cc.8.8.8139.
20. Nakada D, Saunders TL, Morrison SJ. Lkb1 regulates cell cycle and energy metabolism in haematopoietic stem cells. Nature 2010; 468:653-8; PMID:21124450; http://dx.doi.org/10.1038/nature09571.
21. Gan B, Hu J, Jiang S, Liu Y, Sahin E, Zhuang L, et al. Lkb1 regulates quiescence and metabolic homeostasis of haematopoietic stem cells. Nature 2010; 468:701-4; PMID:21124456; http://dx.doi.org/10.1038/nature09595.
22. Gurumurthy S, Xie SZ, Alagesan B, Kim J, Yusuf RZ, Saez B, et al. The Lkb1 metabolic sensor maintains haematopoietic stem cell survival. Nature 2010; 468:659-63; PMID:21124451; http://dx.doi.org/10.1038/nature09572.
23. Yamazaki S, Iwama A, Takayanagi S, Morita Y, Eto K, Ema H, et al. Cytokine signals modulated via lipid rafts mimic niche signals and induce hibernation in hematopoietic stem cells. EMBO J 2006; 25:3515-23; PMID:16858398; http://dx.doi.org/10.1038/sj.emboj.7601236.
24. Yamazaki S, Iwama A, Takayanagi S, Eto K, Ema H, Nakauchi H. TGFbeta as a candidate bone marrow niche signal to induce hematopoietic stem cell hibernation. Blood 2009; 113:1250-6; PMID:18945958; http://dx.doi.org/10.1182/ blood-2008-04-146480.
25. Lingwood D, Simons K. Lipid rafts as a membrane-organizing principle. Science 2010; 327:46- 50; PMID:20044567; http://dx.doi.org/10.1126/science. 1174621.
26. Moran M, Miceli MC. Engagement of GPI-linked CD48 contributes to TCR signals and cytoskeletal reorganization: a role for lipid rafts in T cell activation. Immunity 1998; 9:787-96; PMID:9881969; http://dx.doi.org/10.1016/ S1074-7613(00)80644-5.
27. Jahn T, Leifheit E, Gooch S, Sindhu S, Weinberg K. Lipid rafts are required for Kit survival and proliferation signals. Blood 2007; 110:1739-47; PMID:17554062; http://dx.doi.org/10.1182/blood-2006-05-020925.
28. Bullock TE, Wen B, Marley SB, Gordon MY. Potential of CD34 in the regulation of symmetrical and asymmetrical divisions by hematopoietic progenitor cells. Stem Cells 2007; 25:844-51; PMID:17185613; http://dx.doi.org/10.1634/ stemcells.2006-0346.
29. 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; 121:1109-21; PMID:15989959; http://dx.doi.org/10.1016/j.cell.2005.05.026.
30. 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; 27:2498-508; PMID:19593793; http://dx.doi.org/10. 1002/stem.170.
31. Matthias P, Lutolf RD, Havenstrite K, Koleckar K, Blau HM. Perturbation of single hematopoietic stem cell fates in artificial niches. Integr Biol 2009; 1:59-69; http://dx.doi.org/10.1039/b815718a.
32. Wilson A, Laurenti E, Oser G, van der Wath RC, Blanco-Bose W, Jaworski M, et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008; 135:1118-29; PMID:19062086; http://dx.doi.org/10.1016/j.cell.2008.10.048.
33. Eilken HM, Nishikawa S, Schroeder T. Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 2009; 457:896-900; PMID:19212410; http://dx.doi.org/10.1038/nature07760.
34. Kobel S, Limacher M, Gobaa S, Laroche T, Lutolf MP. Micropatterning of hydrogels by soft embossing. Langmuir 2009; 25:8774-9; PMID:19361170; http://dx.doi.org/10.1021/la9002115.
35. Metcalf D, Di Rago L, Mifsud S. Synergistic and inhibitory interactions in the in vitro control of murine megakaryocyte colony formation. Stem Cells 2002; 20:552-60; PMID:12456963; http://dx.doi.org/10.1002/stem.200552.
36. Cheng T, Shen H, Rodrigues N, Stier S, Scadden DT. Transforming growth factor beta 1 mediates cell cycle arrest of primitive hematopoietic cells independent of p21(Cip1/Waf1) or p27(Kip1). Blood 2001; 98:3643-9; PMID:11739168; http://dx.doi.org/10.1182/blood.V98.13.3643.
37. Zacharias DA, Violin JD, Newton AC, Tsien RY. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 2002; 296:913-6; PMID:11988576; http://dx.doi.org/10.1126/science.1068539.
38. Gillette JM, Larochelle A, Dunbar CE, Lippincott-Schwartz J. Intercellular transfer to signalling endosomes regulates an ex vivo bone marrow niche. Nat Cell Biol 2009; 11:303-11; PMID:19198600; http://dx.doi.org/10.1038/ ncb1838.
39. Szafer-Glusman E, Giansanti MG, Nishihama R, Bolival B, Pringle J, Gatti M, et al. A role for very-long-chain fatty acids in furrow ingression during cytokinesis in Drosophila spermatocytes. Curr Biol 2008; 18:1426-31; PMID:18804373; http://dx.doi.org/10.1016/j.cub.2008.08.061.
40. Skop AR, Liu H, Yates J, 3rd, Meyer BJ, Heald R. Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science 2004; 305:61-6; PMID:15166316; http://dx.doi.org/10.1126/science.1097931.
41. Cobas M, Wilson A, Ernst B, Mancini SJ, MacDonald HR, Kemler R, et al. Beta-catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med 2004; 199:221-9; PMID:14718516; http://dx.doi.org/10.1084/jem.20031615.
42. Jeannet G, Scheller M, Scarpellino L, Duboux S, Gardiol N, Back J, et al. Long-term, multilineage hematopoiesis occurs in the combined absence of beta-catenin and gamma-catenin. Blood 2008; 111:142-9; PMID:17906078; http://dx.doi.org/10.1182/blood-2007-07-102558.
43. Scheller M, Huelsken J, Rosenbauer F, Taketo MM, Birchmeier W, Tenen DG, et al. Hematopoietic stem cell and multilineage defects generated by constitutive beta-catenin activation. Nat Immunol 2006; 7:1037-47; PMID:16951686; http://dx.doi.org/10.1038/ni1387.
44. Kirstetter P, Anderson K, Porse BT, Jacobsen SE, Nerlov C. Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block. Nat Immunol 2006; 7:1048-56; PMID:16951689; http://dx.doi.org/10.1038/ni1381.
45. Fleming HE, Janzen V, Lo Celso C, Guo J, Leahy KM, Kronenberg HM, et al. Wnt signaling in the niche enforces hematopoietic stem cell quiescence and is necessary to preserve self-renewal in vivo. Cell Stem Cell 2008; 2:274-83; PMID:18371452; http://dx.doi.org/10.1016/j.stem.2008.01.003.
46. Peters SO, Kittler EL, Ramshaw HS, Quesenberry PJ. Ex vivo expansion of murine marrow cells with interleukin-3 (IL-3), IL-6, IL-11 and stem cell factor leads to impaired engraftment in irradiated hosts. Blood 1996; 87:30-7; PMID:8547656.
47. Habibian HK, Peters SO, Hsieh CC, Wuu J, Vergilis K, Grimaldi CI, et al. The fluctuating phenotype of the lymphohematopoietic stem cell with cell cycle transit. J Exp Med 1998; 188:393-8; PMID:9670051; http://dx.doi.org/10.1084/jem. 188.2.393.
48. Sanchez-Garcia J, Torres A, Herrera C, Alvarez MA. Cell cycle kinetic changes induced by interleukin-3 and interleukin-6 during ex vivo expansion of mobilized peripheral blood CD34 cells. Haematologica 2006; 91:121-4; PMID:16434380.
49. Irion S, Clarke RL, Luche H, Kim I, Morrison SJ, Fehling HJ, et al. Temporal specification of blood progenitors from mouse embryonic stem cells and induced pluripotent stem cells. Development 2010; 137:2829-39; PMID:20659975; http://dx.doi.org/10.1242/dev.042119.
50. Pitchford SC, Furze RC, Jones CP, Wengner AM, Rankin SM. Differential mobilization of subsets of progenitor cells from the bone marrow. Cell Stem Cell 2009; 4:62-72; PMID:19128793; http://dx.doi.org/10.1016/j.stem.2008.10.017.
51. Kolonin MG, Simmons PJ. Combinatorial stem cell mobilization. Nat Biotechnol 2009; 27:252-3; PMID:19270674; http://dx.doi.org/10.1038/nbt0309-252.
52. Lasserre R, Guo XJ, Conchonaud F, Hamon Y, Hawchar O, Bernard AM, et al. Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat Chem Biol 2008; 4:538-47; PMID:18641634; http://dx.doi.org/10. 1038/nchembio.103.
53. Miyamoto K, Araki KY, Naka K, Arai F, Takubo K, Yamazaki S, et al. Foxo3a is essential for maintenance of the hematopoietic stem cell pool. Cell Stem Cell 2007; 1:101-12; PMID:18371339; http://dx.doi.org/10.1016/j.stem.2007.02. 001.
54. Ko KH, Holmes T, Palladinetti P, Song E, Nordon R, O'Brien TA, et al. GSK-3beta Inhibition Promotes Engraftment of Ex Vivo Expanded Hematopoietic Stem Cells and Modulates Gene Expression. Stem Cells 2010; PMID:20960517.
55. Chen C, Liu Y, Liu R, Ikenoue T, Guan KL, Liu Y, et al. TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J Exp Med 2008; 205:2397-408; PMID:18809716; http://dx.doi.org/10.1084/jem.20081297.
56. Fortunel NO, Hatzfeld A, Hatzfeld JA. Transforming growth factorbeta: pleiotropic role in the regulation of hematopoiesis. Blood 2000; 96:2022-36; PMID:10979943.