The endothelial antigen ESAM monitors hematopoietic stem cell status between quiescence and self-renewal

Journal of Immunology

Volumn 189, Issue 1, 2012, Pages 200-210

  Sudo, Takao ^a   Yokota, Takafumi ^a   Oritani, Kenji ^a   Satoh, Yusuke ^a   Sugiyama, Tatsuki ^b   Ishida, Tatsuro ^c   Shibayama, Hirohiko ^a   Ezoe, Sachiko ^a   Fujita, Natsuko ^a   Tanaka, Hirokazu ^a,d   Maeda, Tetsuo ^a   Nagasawa, Takashi ^b   Kanakura, Yuzuru ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d KINKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; DNA TOPOISOMERASE (ATP HYDROLYSING); ENDOTHELIAL CELL SELECTIVE ADHESION MOLECULE; FLUOROURACIL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BONE MARROW; BONE MARROW SUPPRESSION; CELL ACTIVATION; CELL CYCLE; CELL ISOLATION; CELL RENEWAL; CONTROLLED STUDY; FLOW CYTOMETRY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS; BIOLOGICAL MARKERS; BONE MARROW CELLS; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELL LINE; ENDOTHELIUM, VASCULAR; G0 PHASE; HEMATOPOIETIC STEM CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT;

EID: 84862851181     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200056     Document Type: Article

References (57)

1. Kiel, M. J., O. H. Yilmaz, T. Iwashita, O. H. Yilmaz, C. Terhorst, and S. J. Morrison. 2005. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121: 1109-1121. (Pubitemid 40884400)
2. Osawa, M., K. Hanada, H. Hamada, and H. Nakauchi. 1996. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273: 242-245. (Pubitemid 26285891)
3. Spangrude, G. J., S. Heimfeld, and I. L. Weissman. 1988. Purification and characterization of mouse hematopoietic stem cells. Science 241: 58-62.
4. Foudi, A., K. Hochedlinger, D. Van Buren, J. W. Schindler, R. Jaenisch, V. Carey, and H. Hock. 2009. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat. Biotechnol. 27: 84-90.
5. Wilson, A., E. Laurenti, G. Oser, R. C. van der Wath, W. Blanco-Bose, M. Jaworski, S. Offner, C. F. Dunant, L. Eshkind, E. Bockamp, et al. 2008. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 135: 1118-1129.
6. Ema, H., and H. Nakauchi. 2000. Expansion of hematopoietic stem cells in the developing liver of a mouse embryo. Blood 95: 2284-2288. (Pubitemid 30167726)
7. Bowie, M. B., D. G. Kent, B. Dykstra, K. D. McKnight, L. McCaffrey, P. A. Hoodless, and C. J. Eaves. 2007. Identification of a new intrinsically timed developmental checkpoint that reprograms key hematopoietic stem cell properties. Proc. Natl. Acad. Sci. USA 104: 5878-5882. (Pubitemid 47175627)
8. Randall, T. D., and I. L. Weissman. 1997. Phenotypic and functional changes induced at the clonal level in hematopoietic stem cells after 5-fluorouracil treatment. Blood 89: 3596-3606. (Pubitemid 27227082)
9. Li, L., and H. Clevers. 2010. Coexistence of quiescent and active adult stem cells in mammals. Science 327: 542-545.
10. Wilson, A., and A. Trumpp. 2006. Bone-marrow haematopoietic-stem-cell niches. Nat. Rev. Immunol. 6: 93-106. (Pubitemid 43361585)
11. Hirata Ki, T., K. Ishida, M. Penta, E. Rezaee, J. Yang, Wohlgemuth, and T. Quertermous. 2001. Cloning of an immunoglobulin family adhesion molecule selectively expressed by endothelial cells. J. Biol. Chem. 276: 16223-16231.
12. Nasdala, I., K. Wolburg-Buchholz, H. Wolburg, A. Kuhn, K. Ebnet, G. Brachtendorf, U. Samulowitz, B. Kuster, B. Engelhardt, D. Vestweber, and S. Butz. 2002. A transmembrane tight junction protein selectively expressed on endothelial cells and platelets. J. Biol. Chem. 277: 16294-16303. (Pubitemid 34967918)
13. Wegmann, F., B. Petri, A. G. Khandoga, C. Moser, A. Khandoga, S. Volkery, H. Li, I. Nasdala, O. Brandau, R. Fässler, et al. 2006. ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J. Exp. Med. 203: 1671-1677. (Pubitemid 44036272)
14. Hara, T., T. Ishida, H. M. Cangara, and K. Hirata. 2009. Endothelial cell-selective adhesion molecule regulates albuminuria in diabetic nephropathy. Microvasc. Res. 77: 348-355.
15. Stalker, T. J., J. Wu, A. Morgans, E. A. Traxler, L. Wang, M. S. Chatterjee, D. Lee, T. Quertermous, R. A. Hall, D. A. Hammer, et al. 2009. Endothelial cell specific adhesion molecule (ESAM) localizes to platelet-platelet contacts and regulates thrombus formation in vivo. J. Thromb. Haemost. 7: 1886-1896.
16. Yokota, T., K. Oritani, S. Butz, K. Kokame, P. W. Kincade, T. Miyata, D. Vestweber, and Y. Kanakura. 2009. The endothelial antigen ESAM marks primitive hematopoietic progenitors throughout life in mice. Blood 113: 2914-2923.
17. Ogawa, M. 2002. Changing phenotypes of hematopoietic stem cells. Exp. Hematol. 30: 3-6. (Pubitemid 34059211)
18. Ishida, T., R. K. Kundu, E. Yang, K. Hirata, Y. D. Ho, and T. Quertermous. 2003. Targeted disruption of endothelial cell-selective adhesion molecule inhibits angiogenic processes in vitro and in vivo. J. Biol. Chem. 278: 34598-34604. (Pubitemid 37553309)
19. Inoue, M., T. Ishida, T. Yasuda, R. Toh, T. Hara, H. M. Cangara, Y. Rikitake, K. Taira, L. Sun, R. K. Kundu, et al. 2010. Endothelial cell-selective adhesion molecule modulates atherosclerosis through plaque angiogenesis and monocyte-endothelial interaction. Microvasc. Res. 80: 179-187.
20. Harrison, D. E., C. T. Jordan, R. K. Zhong, and C. M. Astle. 1993. Primitive hemopoietic stem cells: direct assay of most productive populations by competitive repopulation with simple binomial, correlation and covariance calculations. Exp. Hematol. 21: 206-219. (Pubitemid 24216758)
21. Sugiyama, T., H. Kohara, M. Noda, and T. Nagasawa. 2006. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25: 977-988. (Pubitemid 44894948)
22. Yilmaz, O. H., M. J. Kiel, and S. J. Morrison. 2006. SLAM family markers are conserved among hematopoietic stem cells from old and reconstituted mice and markedly increase their purity. Blood 107: 924-930. (Pubitemid 43156288)
23. Arai, F., and T. Suda. 2007. Maintenance of quiescent hematopoietic stem cells in the osteoblastic niche. Ann. N. Y. Acad. Sci. 1106: 41-53. (Pubitemid 47443041)
24. Lerner, C., and D. E. Harrison. 1990. 5-Fluorouracil spares hemopoietic stem cells responsible for long-term repopulation. Exp. Hematol. 18: 114-118. (Pubitemid 20072292)
25. Yin, T., and L. Li. 2006. The stem cell niches in bone. J. Clin. Invest. 116: 1195-1201.
26. Morita, Y., H. Ema, and H. Nakauchi. 2010. Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment. J. Exp. Med. 207: 1173-1182.
27. Wang, C. Y., J. C. Cusack, Jr., R. Liu, and A. S. Baldwin, Jr. 1999. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-κB. Nat. Med. 5: 412-417. (Pubitemid 29180579)
28. Spitzner, J. R., and M. T. Muller. 1988. A consensus sequence for cleavage by vertebrate DNA topoisomerase II. Nucleic Acids Res. 16: 5533-5556.
29. Tumbar, T., G. Guasch, V. Greco, C. Blanpain, W. E. Lowry, M. Rendl, and E. Fuchs. 2004. Defining the epithelial stem cell niche in skin. Science 303: 359-363. (Pubitemid 38095773)
30. Harrison, D. E., and C. P. Lerner. 1991. Most primitive hematopoietic stem cells are stimulated to cycle rapidly after treatment with 5-fluorouracil. Blood 78: 1237-1240.
31. Haug, J. S., X. C. He, J. C. Grindley, J. P. Wunderlich, K. Gaudenz, J. T. Ross, A. Paulson, K. P. Wagner, Y. Xie, R. Zhu, et al. 2008. N-cadherin expression level distinguishes reserved versus primed states of hematopoietic stem cells. Cell Stem Cell 2: 367-379. (Pubitemid 351455240)
32. Sirin, O., G. L. Lukov, R. Mao, O. M. Conneely, and M. A. Goodell. 2010. The orphan nuclear receptor Nurr1 restricts the proliferation of haematopoietic stem cells. Nat. Cell Biol. 12: 1213-1219.
33. Venezia, T. A., A. A. Merchant, C. A. Ramos, N. L. Whitehouse, A. S. Young, C. A. Shaw, and M. A. Goodell. 2004. Molecular signatures of proliferation and quiescence in hematopoietic stem cells. PLoS Biol. 2: e301.
34. - cells are transiently reconstituting multipotent progenitors with little or no stem cell activity. Blood 111: 4413-4414, author reply 4414-4415.
35. - side population cells represent a functionally distinct population of long-term hematopoietic stem cells. Blood 111: 2444-2451.
36. Passegué, E., A. J. Wagers, S. Giuriato, W. C. Anderson, and I. L. Weissman. 2005. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J. Exp. Med. 202: 1599-1611. (Pubitemid 41746605)
37. Steinman, R. A. 2002. Cell cycle regulators and hematopoiesis. Oncogene 21: 3403-3413. (Pubitemid 34587712)
38. + cells in NOD/SCID mice. Blood 96: 2100-2107.
39. Lo Celso, C., H. E. Fleming, J. W. Wu, C. X. Zhao, S. Miake-Lye, J. Fujisaki, D. Côté, D. W. Rowe, C. P. Lin, and D. T. Scadden. 2009. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 457: 92-96.
40. Xie, Y., T. Yin, W. Wiegraebe, X. C. He, D. Miller, D. Stark, K. Perko, R. Alexander, J. Schwartz, J. C. Grindley, et al. 2009. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 457: 97-101.
41. Katayama, Y., M. Battista, W. M. Kao, A. Hidalgo, A. J. Peired, S. A. Thomas, and P. S. Frenette. 2006. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124: 407-421. (Pubitemid 43121987)
42. Yamazaki, S., H. Ema, G. Karlsson, T. Yamaguchi, H. Miyoshi, S. Shioda, M. M. Taketo, S. Karlsson, A. Iwama, and H. Nakauchi. 2011. Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147: 1146-1158.
43. Cheng, J., S. Baumhueter, G. Cacalano, K. Carver-Moore, H. Thibodeaux, R. Thomas, H. E. Broxmeyer, S. Cooper, N. Hague, M. Moore, and L. A. Lasky. 1996. Hematopoietic defects in mice lacking the sialomucin CD34. Blood 87: 479-490. (Pubitemid 26030303)
44. Ooi, A. G., H. Karsunky, R. Majeti, S. Butz, D. Vestweber, T. Ishida, T. Quertermous, I. L. Weissman, and E. C. Forsberg. 2009. The adhesion molecule Esam1 is a novel hematopoietic stem cell marker. Stem Cells 27: 653-661.
45. Fonseca, A. V., D. Freund, M. Bornhäuser, and D. Corbeil. 2010. Polarization and migration of hematopoietic stem and progenitor cells rely on the RhoA/ROCK I pathway and an active reorganization of the microtubule network. J. Biol. Chem. 285: 31661-31671.
46. 1-to-S-phase transition. Mol. Cell. Biol. 19: 2690-2698.
47. Hossain, M. S., N. Akimitsu, T. Takaki, H. Hirai, and K. Sekimizu. 2002. ICRF-193, a catalytic inhibitor of DNA topoisomerase II, inhibits re-entry into the cell division cycle from quiescent state in mammalian cells. Genes Cells 7: 285-294. (Pubitemid 34257662)
48. Ju, B. G., V. V. Lunyak, V. Perissi, I. Garcia-Bassets, D. W. Rose, C. K. Glass, and M. G. Rosenfeld. 2006. A topoisomerase IIβ-mediated dsDNA break required for regulated transcription. Science 312: 1798-1802. (Pubitemid 43962898)
49. Jang, Y. Y., and S. J. Sharkis. 2007. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 110: 3056-3063.
50. Orford, K. W., and D. T. Scadden. 2008. Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat. Rev. Genet. 9: 115-128.
51. Morgan, M. J., and Z. G. Liu. 2011. Crosstalk of reactive oxygen species and NF-κB signaling. Cell Res. 21: 103-115.
52. Ito, K., A. Hirao, F. Arai, S. Matsuoka, K. Takubo, I. Hamaguchi, K. Nomiyama, K. Hosokawa, K. Sakurada, N. Nakagata, et al. 2004. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431: 997-1002. (Pubitemid 39434422)
53. Liu, J., L. Cao, J. Chen, S. Song, I. H. Lee, C. Quijano, H. Liu, K. Keyvanfar, H. Chen, L. Y. Cao, et al. 2009. Bmi1 regulates mitochondrial function and the DNA damage response pathway. Nature 459: 387-392.
54. Tothova, Z., R. Kollipara, B. J. Huntly, B. H. Lee, D. H. Castrillon, D. E. Cullen, E. P. McDowell, S. Lazo-Kallanian, I. R. Williams, C. Sears, et al. 2007. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128: 325-339. (Pubitemid 46137992)
55. Kim, M., H. B. Moon, and G. J. Spangrude. 2003. Major age-related changes of mouse hematopoietic stem/progenitor cells. Ann. N. Y. Acad. Sci. 996: 195-208. (Pubitemid 36706601)
56. Morrison, S. J., A. M. Wandycz, K. Akashi, A. Globerson, and I. L. Weissman. 1996. The aging of hematopoietic stem cells. Nat. Med. 2: 1011-1016. (Pubitemid 26306840)
57. Sudo, K., H. Ema, Y. Morita, and H. Nakauchi. 2000. Age-associated characteristics of murine hematopoietic stem cells. J. Exp. Med. 192: 1273-1280.