The Wnt agonist R-spondin1 regulates systemic graft-versus-host disease by protecting intestinal stem cells

Journal of Experimental Medicine

Volumn 208, Issue 2, 2011, Pages 285-294

  Takashima, Shuichiro ^a   Kadowaki, Masanori ^a   Aoyama, Kazutoshi ^a   Koyama, Motoko ^a   Oshima, Takeshi ^b   Tomizuka, Kazuma ^b   Akashi, Koichi ^a   Teshima, Takanori ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KYOWA HAKKO KOGYO CO LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN R SPONDIN1; UNCLASSIFIED DRUG; WNT PROTEIN;

ALLOGENIC BONE MARROW TRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL PROTECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIGESTIVE SYSTEM INJURY; FEMALE; GRAFT VERSUS HOST REACTION; INTESTINE CELL; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; TREATMENT OUTCOME;

ANIMALS; BONE MARROW TRANSPLANTATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GRAFT VS HOST DISEASE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTESTINAL MUCOSA; MICE; POLYMERASE CHAIN REACTION; REGENERATION; SIGNAL TRANSDUCTION; STATISTICS, NONPARAMETRIC; STEM CELLS; THROMBOSPONDINS; WNT PROTEINS;

EID: 79951698988     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20101559     Document Type: Article

References (39)

1. Antin, J.H., S.J. Lee, D. Neuberg, E. Alyea, R.J. Soiffer, S. Sonis, and J.L. Ferrara. 2002. A phase I/II double-blind, placebo-controlled study of recombinant human interleukin-11 for mucositis and acute GVHD prevention in allogeneic stem cell transplantation. Bone Marrow Transplant. 29:373-377. doi:10.1038/sj.bmt.1703394 (Pubitemid 34262638)
2. Asakura, S., D. Hashimoto, S. Takashima, H. Sugiyama, Y. Maeda, K. Akashi, M. Tanimoto, and T. Teshima. 2010. Alloantigen expression on non-hematopoietic cells reduces graft-versus-leukemia effects in mice. J. Clin. Invest. 120:2370-2378. doi:10.1172/JCI39165
3. Barker, N., J.H. van Es, J. Kuipers, P. Kujala, M. van den Born, M. Cozijnsen, A. Haegebarth, J. Korving, H. Begthel, P.J. Peters, and H. Clevers. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 449:1003-1007. doi:10.1038/nature06196 (Pubitemid 350014593)
4. Barker, N., M. van de Wetering, and H. Clevers. 2008. The intestinal stem cell. Genes Dev. 22:1856-1864. doi:10.1101/gad.1674008 (Pubitemid 352008634)
5. Batlle, E., J.T. Henderson, H. Beghtel, M.M. van den Born, E. Sancho, G. Huls, J. Meeldijk, J. Robertson, M. van de Wetering, T. Pawson, and H. Clevers. 2002. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell. 111:251-263. doi:10.1016/S0092-8674(02)01015-2 (Pubitemid 35292445)
6. Bhanja, P., S. Saha, R. Kabarriti, L. Liu, N. Roy-Chowdhury, J. Roy-Chowdhury, R.S. Sellers, A.A. Alfieri, and C. Guha. 2009. Protective role of R-spondin1, an intestinal stem cell growth factor, against radiation-induced gastrointestinal syndrome in mice. PLoS One. 4:e8014. doi:10.1371/journal.pone. 0008014
7. Binnerts, M.E., K.A. Kim, J.M. Bright, S.M. Patel, K. Tran, M. Zhou, J.M. Leung, Y. Liu, W.E. Lomas III, M. Dixon, et al. 2007. R-Spondin1 regulates Wnt signaling by inhibiting internalization of LRP6. Proc. Natl. Acad. Sci. USA. 104:14700-14705. doi:10.1073/pnas.0702305104 (Pubitemid 350003206)
8. Blazar, B.R., D.J. Weisdorf, T. Defor, A. Goldman, T. Braun, S. Silver, and J.L. Ferrara. 2006. Phase 1/2 randomized, placebo-control trial of palifermin to prevent graft-versus-host disease (GVHD) after allogeneic hematopoietic stem cell transplantation (HSCT). Blood. 108:3216-3222. doi:10.1182/blood-2006-04-017780
9. Cooke, K.R., G.R. Hill, J.M. Crawford, D. Bungard, Y.S. Brinson, J. Delmonte Jr., and J.L. Ferrara. 1998. Tumor necrosis factor- alpha production to lipopolysaccharide stimulation by donor cells predicts the severity of experimental acute graft-versus-host disease. J. Clin. Invest. 102:1882-1891. doi:10.1172/JCI4285 (Pubitemid 28533836)
10. Cooke, K.R., A. Gerbitz, J.M. Crawford, T. Teshima, G.R. Hill, A. Tesolin, D.P. Rossignol, and J.L. Ferrara. 2001. LPS antagonism reduces graft-versus-host disease and preserves graft-versus-leukemia activity after experimental bone marrow transplantation. J. Clin. Invest. 107:1581-1589. doi:10.1172/JCI12156 (Pubitemid 32574644)
11. Ding, Y., S. Shen, A.C. Lino, M.A. Curotto de Lafaille, and J.J. Lafaille. 2008. Beta-catenin stabilization extends regulatory T cell survival and induces anergy in nonregulatory T cells. Nat. Med. 14:162-169. doi:10.1038/nm1707 (Pubitemid 351214554)
12. Epstein, R.J., G.B. McDonald, G.E. Sale, H.M. Shulman, and E.D. Thomas. 1980. The diagnostic accuracy of the rectal biopsy in acute graft-versus-host disease: a prospective study of thirteen patients. Gastroenterology. 78:764-771. (Pubitemid 10107919)
13. Farrell, C.L., J.V. Bready, K.L. Rex, J.N. Chen, C.R. DiPalma, K.L. Whitcomb, S. Yin, D.C. Hill, B. Wiemann, C.O. Starnes, et al. 1998. Keratinocyte growth factor protects mice from chemotherapy and radiation-induced gastrointestinal injury and mortality. Cancer Res. 58:933-939. (Pubitemid 28182461)
14. Ferrara, J.L., K.R. Cooke, and T. Teshima. 2003. The pathophysiology of acute graft-versus-host disease. Int. J. Hematol. 78:181-187. doi:10.1007/BF02983793 (Pubitemid 37288503)
15. Gattinoni, L., X.S. Zhong, D.C. Palmer, Y. Ji, C.S. Hinrichs, Z. Yu, C. Wrzesinski, A. Boni, L. Cassard, L.M. Garvin, et al. 2009. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat. Med. 15:808-813. doi:10.1038/nm.1982
16. Hill, G.R., and J.L. Ferrara. 2000. The primacy of the gastrointestinal tract as a target organ of acute graft-versus-host disease: rationale for the use of cytokine shields in allogeneic bone marrow transplantation. Blood. 95:2754-2759. (Pubitemid 30235880)
17. Hill, G.R., J.M. Crawford, K.R. Cooke, Y.S. Brinson, L. Pan, and J.L. Ferrara. 1997. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood. 90:3204-3213. (Pubitemid 27444217)
18. Hill, G.R., K.R. Cooke, T. Teshima, J.M. Crawford, J.C. Keith Jr., Y.S. Brinson, D. Bungard, and J.L. Ferrara. 1998. Interleukin-11 promotes T cell polarization and prevents acute graft-versus-host disease after allogeneic bone marrow transplantation. J. Clin. Invest. 102:115-123. doi:10.1172/JCI3132 (Pubitemid 28323837)
19. Kahl, C., B.E. Storer, B.M. Sandmaier, M. Mielcarek, M.B. Maris, K.G. Blume, D. Niederwieser, T.R. Chauncey, S.J. Forman, E. Agura, et al. 2007. Relapse risk in patients with malignant diseases given allogeneic hematopoietic cell transplantation after nonmyeloablative conditioning. Blood. 110:2744-2748. doi:10.1182/blood-2007-03-078592 (Pubitemid 47523200)
20. Kim, K.A., M. Kakitani, J. Zhao, T. Oshima, T. Tang, M. Binnerts, Y. Liu, B. Boyle, E. Park, P. Emtage, et al. 2005. Mitogenic influence of human R-spondin1 on the intestinal epithelium. Science. 309:1256-1259. doi:10.1126/science.1112521 (Pubitemid 41170922)
21. Kim, K.A., J. Zhao, S. Andarmani, M. Kakitani, T. Oshima, M.E. Binnerts, A. Abo, K. Tomizuka, and W.D. Funk. 2006. R-Spondin proteins: a novel link to beta-catenin activation. Cell Cycle. 5:23-26. doi:10.4161/cc.5.1.2305
22. Krijanovski, O.I., G.R. Hill, K.R. Cooke, T. Teshima, J.M. Crawford, Y.S. Brinson, and J.L. Ferrara. 1999. Keratinocyte growth factor separates graft-versus-leukemia effects from graft-versus-host disease. Blood. 94:825-831. (Pubitemid 29323898)
23. Mori, T., T. Nishimura, Y. Ikeda, T. Hotta, H. Yagita, and K. Ando. 1998. Involvement of Fas-mediated apoptosis in the hematopoietic progenitor cells of graft-versus-host reaction-associated myelosuppression. Blood. 92:101-107. (Pubitemid 28303181)
24. Mowat, M., and G. Socie. 2004. Intestinal Graft-vs.-Host Disease. In Graftvs.-Host Disease. Third edition. J.L. Ferrara, K.R. Cooke, and H.J. Deeg, editors. Marcel Dekker, New York. 279-327.
25. Nestel, F.P., K.S. Price, T.A. Seemayer, and W.S. Lapp. 1992. Macrophage priming and lipopolysaccharide-triggered release of tumor necrosis factor alpha during graft-versus-host disease. J. Exp. Med. 175:405-413. doi:10.1084/jem.175. 2.405
26. Panoskaltsis-Mortari, A., D.L. Lacey, D.A. Vallera, and B.R. Blazar. 1998. Keratinocyte growth factor administered before conditioning ameliorates graft-versus-host disease after allogeneic bone marrow transplantation in mice. Blood. 92:3960-3967. (Pubitemid 28525223)
27. Pinto, D., A. Gregorieff, H. Begthel, and H. Clevers. 2003. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev. 17:1709-1713. doi:10.1101/gad.267103 (Pubitemid 36870334)
28. Reya, T., and H. Clevers. 2005. Wnt signalling in stem cells and cancer. Nature. 434:843-850. doi:10.1038/nature03319 (Pubitemid 40558990)
29. Román-Gómez, J., L. Cordeu, X. Agirre, A. Jiménez-Velasco, E. San José-Eneriz, L. Garate, M.J. Calasanz, A. Heiniger, A. Torres, and F. Prosper. 2007. Epigenetic regulation of Wnt-signaling pathway in acute lymphoblastic leukemia. Blood. 109:3462-3469. doi:10.1182/blood-2006-09-047043 (Pubitemid 46572536)
30. Sale, G.E., H.M. Shulman, G.B. McDonald, and E.D. Thomas. 1979. Gastrointestinal graft-versus-host disease in man. A clinicopathologic study of the rectal biopsy. Am. J. Surg. Pathol. 3:291-299. doi:10.1097/00000478- 197908000-00001 (Pubitemid 9228784)
31. Sato, T., R.G. Vries, H.J. Snippert, M. van de Wetering, N. Barker, D.E. Stange, J.H. van Es, A. Abo, P. Kujala, P.J. Peters, and H. Clevers. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 459:262-265. doi:10.1038/nature07935
32. Teshima, T., G.R. Hill, L. Pan, Y.S. Brinson, M.R. van den Brink, K.R. Cooke, and J.L. Ferrara. 1999. IL-11 separates graft-versus-leukemia effects from graft-versus-host disease after bone marrow transplantation. J. Clin. Invest. 104:317-325. doi:10.1172/JCI7111
33. Teshima, T., R. Ordemann, P. Reddy, S. Gagin, C. Liu, K.R. Cooke, and J.L. Ferrara. 2002a. Acute graft-versus-host disease does not require alloantigen expression on host epithelium. Nat. Med. 8:575-581. doi:10.1038/nm0602-575 (Pubitemid 34633434)
34. Teshima, T., P. Reddy, K.P. Lowler, M.A. KuKuruga, C. Liu, K.R. Cooke, and J.L. Ferrara. 2002b. Flt3 ligand therapy for recipients of allogeneic bone marrow transplants expands host CD8 alpha(+) dendritic cells and reduces experimental acute graft-versus-host disease. Blood. 99:1825-1832. doi:10.1182/blood.V99.5.1825 (Pubitemid 34533059)
35. van der Flier, L.G., A. Haegebarth, D.E. Stange, M. van de Wetering, and H. Clevers. 2009a. OLFM4 is a robust marker for stem cells in human intestine and marks a subset of colorectal cancer cells. Gastroenterology. 137:15-17. doi:10.1053/j.gastro.2009.05.035
36. van der Flier, L.G., M.E. van Gijn, P. Hatzis, P. Kujala, A. Haegebarth, D.E. Stange, H. Begthel, M. van den Born, V. Guryev, I. Oving, et al. 2009b. Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell. 136:903-912. doi:10.1016/j.cell.2009.01.031
37. Via, C.S., S.O. Sharrow, and G.M. Shearer. 1987. Role of cytotoxic T lymphocytes in the prevention of lupus-like disease occurring in a murine model of graft-vs-host disease. J. Immunol. 139:1840-1849. (Pubitemid 17141612)
38. Zhao, J., J. de Vera, S. Narushima, E.X. Beck, S. Palencia, P. Shinkawa, K.A. Kim, Y. Liu, M.D. Levy, D.J. Berg, et al. 2007. R-spondin1, a novel intestinotrophic mitogen, ameliorates experimental colitis in mice. Gastroenterology. 132:1331-1343. doi:10.1053/j.gastro.2007.02.001
39. Zhao, J., K.A. Kim, J. De Vera, S. Palencia, M. Wagle, and A. Abo. 2009. R-Spondin1 protects mice from chemotherapy or radiation-induced oral mucositis through the canonical Wnt/beta-catenin pathway. Proc. Natl. Acad. Sci. USA. 106:2331-2336. doi:10.1073/pnas.0805159106