GM-CSF produced by nonhematopoietic cells is required for early epithelial cell proliferation and repair of injured colonic mucosa

Journal of Immunology

Volumn 190, Issue 4, 2013, Pages 1702-1713

  Egea, Laia ^a   Christopher S McAllister, ^a   Lakhdari, Omar ^a   Minev, Ivelina ^a   Shenouda, Steve ^a   Kagnoff, Martin F ^a,b,c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL PROLIFERATION; CELL REGENERATION; COLITIS; COLON MUCOSA; CONTROLLED STUDY; CRYPT CELL; DISEASE SEVERITY; GENE; GENE EXPRESSION PROFILING; IN VIVO STUDY; INTESTINE ULCER; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REGIII BETA GENE; REGIII GAMA GENE; ULCER HEALING; WILD TYPE; WOUND HEALING;

ANIMALS; BONE MARROW CELLS; CELL PROLIFERATION; COLITIS, ULCERATIVE; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HEMATOPOIESIS; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN CULTURE TECHNIQUES; RADIATION CHIMERA; TIME FACTORS; WOUND HEALING;

EID: 84873542232     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202368     Document Type: Article

References (43)

1. Hamilton, J. A. 2008. Colony-stimulating factors in inflammation and autoimmunity. Nat. Rev. Immunol. 8: 533-544.
2. Martinez-Moczygemba, M., and D. P. Huston. 2003. Biology of common beta receptor-signaling cytokines: IL-3, IL-5, and GM-CSF. J. Allergy Clin. Immunol. 112: 653-665, quiz 666.
3. Egea, L., Y. Hirata, and M. F. Kagnoff. 2010. GM-CSF: a role in immune and inflammatory reactions in the intestine. Expert Rev. Gastroenterol. Hepatol. 4: 723-731.
4. Sennikov, S. V., V. V. Temchura, V. A. Trufakin, and V. A. Kozlov. 2002. Effects of granulocyte-macrophage colony-stimulating factor produced by intestinal epithelial cells on functional activity of hemopoietic stem cells. Bull. Exp. Biol. Med. 134: 548-550.
5. Sennikov, S. V., V. V. Temchura, V. A. Kozlov, and V. A. Trufakin. 2002. The influence of conditioned medium from mouse intestinal epithelial cells on the proliferative activity of crypt cells: role of granulocyte-macrophage colonystimulating factor. J. Gastroenterol. 37: 1048-1051.
6. Fukuzawa, H., M. Sawada, T. Kayahara, Y. Morita-Fujisawa, K. Suzuki, H. Seno, S. Takaishi, and T. Chiba. 2003. Identification of GM-CSF in Paneth cells using single-cell RT-PCR. Biochem. Biophys. Res. Commun. 312: 897-902.
7. Hirsch, T., S. Eggstein, S. Frank, E. H. Farthmann, and B. U. von Specht. 1995. Expression of GM-CSF and a functional GM-CSF receptor in the human colon carcinoma cell line SW403. Biochem. Biophys. Res. Commun. 217: 138-143.
8. Trutmann, M., L. Terracciano, C. Noppen, J. Kloth, M. Kaspar, R. Peterli, P. Tondelli, C. Schaeffer, P. Zajac, M. Heberer, and G. C. Spagnoli. 1998. GMCSF gene expression and protein production in human colorectal cancer cell lines and clinical tumor specimens. Int. J. Cancer 77: 378-385.
9. Noguchi, M., N. Hiwatashi, Z. X. Liu, and T. Toyota. 2001. Increased secretion of granulocyte-macrophage colony-stimulating factor in mucosal lesions of inflammatory bowel disease. Digestion 63(Suppl. 1): 32-36.
10. Ina, K., K. Kusugami, T. Hosokawa, A. Imada, T. Shimizu, T. Yamaguchi, M. Ohsuga, K. Kyokane, T. Sakai, Y. Nishio, et al. 1999. Increased mucosal production of granulocyte colony-stimulating factor is related to a delay in neutrophil apoptosis in Inflammatory Bowel disease. J. Gastroenterol. Hepatol. 14: 46-53.
11. Hirata, Y., L. Egea, S. M. Dann, L. Eckmann, and M. F. Kagnoff. 2010. GMCSF-facilitated dendritic cell recruitment and survival govern the intestinal mucosal response to a mouse enteric bacterial pathogen. Cell Host Microbe 7: 151-163.
12. Bogunovic, M., F. Ginhoux, J. Helft, L. Shang, D. Hashimoto, M. Greter, K. Liu, C. Jakubzick, M. A. Ingersoll, M. Leboeuf, et al. 2009. Origin of the lamina propria dendritic cell network. Immunity 31: 513-525.
13. Varol, C., A. Vallon-Eberhard, E. Elinav, T. Aychek, Y. Shapira, H. Luche, H. J. Fehling, W. D. Hardt, G. Shakhar, and S. Jung. 2009. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31: 502-512.
14. Xu, Y., N. H. Hunt, and S. Bao. 2008. The role of granulocyte macrophagecolony-stimulating factor in acute intestinal inflammation. Cell Res. 18: 1220-1229.
15. Han, X., S. Gilbert, K. Groschwitz, S. Hogan, I. Jurickova, B. Trapnell, C. Samson, and J. Gully. 2010. Loss of GM-CSF signalling in non-haematopoietic cells increases NSAID ileal injury. Gut 59: 1066-1078.
16. Okayasu, I., S. Hatakeyama, M. Yamada, T. Ohkusa, Y. Inagaki, and R. Nakaya. 1990. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98: 694-702.
17. Cooper, H. S., S. N. Murthy, R. S. Shah, and D. J. Sedergran. 1993. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab. Invest. 69: 238-249.
18. Strober, W., I. J. Fuss, and R. S. Blumberg. 2002. The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 20: 495-549.
19. Panja, A., S. Goldberg, L. Eckmann, P. Krishen, and L. Mayer. 1998. The regulation and functional consequence of proinflammatory cytokine binding on human intestinal epithelial cells. J. Immunol. 161: 3675-3684.
20. Sainathan, S. K., E. M. Hanna, Q. Gong, K. S. Bishnupuri, Q. Luo, M. Colonna, F. V. White, E. Croze, C. Houchen, S. Anant, and B. K. Dieckgraefe. 2008. Granulocyte macrophage colony-stimulating factor ameliorates DSS-induced experimental colitis. Inflamm. Bowel Dis. 14: 88-99.
21. Bernasconi, E., L. Favre, M. H. Maillard, D. Bachmann, C. Pythoud, H. Bouzourene, E. Croze, S. Velichko, J. Parkinson, P. Michetti, and D. Velin. 2010. Granulocyte-macrophage colony-stimulating factor elicits bone marrowderived cells that promote efficient colonic mucosal healing. Inflamm. Bowel Dis. 16: 428-441.
22. Cakarova, L., L. M. Marsh, J. Wilhelm, K. Mayer, F. Grimminger, W. Seeger, J. Lohmeyer, and S. Herold. 2009. Macrophage tumor necrosis factor-alpha induces epithelial expression of granulocyte-macrophage colony-stimulating factor: impact on alveolar epithelial repair. Am. J. Respir. Crit. Care Med. 180: 521-532.
23. Maaser, C., M. P. Housley, M. Iimura, J. R. Smith, B. A. Vallance, B. B. Finlay, J. R. Schreiber, N. M. Varki, M. F. Kagnoff, and L. Eckmann. 2004. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect. Immun. 72: 3315-3324.
24. Sásik, R., C. H. Woelk, and J. Corbeil. 2004. Microarray truths and consequences. J. Mol. Endocrinol. 33: 1-9.
25. + T cells by exogenous cell-associated antigens. Immunity 17: 211-220.
26. McAllister, C. S., O. Lakhdari, G. Pineton de Chambrun, M. G. Gareau, A. Broquet, G. H. Lee, S. Shenouda, L. Eckmann, and M. F. Kagnoff. 2013. TLR3, TRIF, and caspase 8 determine double-stranded RNA-induced epithelial cell death and survival in vivo. J. Immunol. 190: 418-427.
27. Medema, J. P., and L. Vermeulen. 2011. Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature 474: 318-326.
28. Ogawa, H., K. Fukushima, H. Naito, Y. Funayama, M. Unno, K. Takahashi, T. Kitayama, S.Matsuno, H. Ohtani, S. Takasawa, et al. 2003. Increased expression of HIP/PAP and regenerating gene III in human inflammatory bowel disease and a murine bacterial reconstitution model. Inflamm. Bowel Dis. 9: 162-170.
29. Moucadel, V., P. Soubeyran, S. Vasseur, N. J. Dusetti, J. C. Dagorn, and J. L. Iovanna. 2001. Cdx1 promotes cellular growth of epithelial intestinal cells through induction of the secretory protein PAP I. Eur. J. Cell Biol. 80: 156-163.
30. Bishnupuri, K. S., Q. Luo, J. R. Korzenik, J. O. Henderson, C. W. Houchen, S. Anant, and B. K. Dieckgraefe. 2006. Dysregulation of Reg gene expression occurs early in gastrointestinal tumorigenesis and regulates anti-apoptotic genes. Cancer Biol. Ther. 5: 1714-1720.
31. Jung, H. C., L. Eckmann, S. K. Yang, A. Panja, J. Fierer, E. Morzycka-Wroblewska, and M. F. Kagnoff. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Invest. 95: 55-65.
32. Pickert, G., C. Neufert, M. Leppkes, Y. Zheng, N. Wittkopf, M. Warntjen, H. A. Lehr, S. Hirth, B. Weigmann, S. Wirtz, et al. 2009. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 206: 1465-1472.
33. Wang, L., T. Yi, M. Kortylewski, D. M. Pardoll, D. Zeng, and H. Yu. 2009. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J. Exp. Med. 206: 1457-1464.
34. Hyun, Y. S., D. S. Han, A. R. Lee, C. S. Eun, J. Youn, and H. Y. Kim. 2012. Role of IL-17A in the development of colitis-associated cancer. Carcinogenesis 33: 931-936.
35. Dieleman, L. A., M. J. Palmen, H. Akol, E. Bloemena, A. S. Peña, S. G. Meuwissen, and E. P. Van Rees. 1998. Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin. Exp. Immunol. 114: 385-391.
36. Fleetwood, A. J., A. D. Cook, and J. A. Hamilton. 2005. Functions of granulocytemacrophage colony-stimulating factor. Crit. Rev. Immunol. 25: 405-428.
37. Hamilton, J. A. 2002. GM-CSF in inflammation and autoimmunity. Trends Immunol. 23: 403-408.
38. Goldstein, J. I., D. J. Kominsky, N. Jacobson, B. Bowers, K. Regalia, G. L. Austin, M. Yousefi, M. T. Falta, A. P. Fontenot, M. E. Gerich, et al. 2011. Defective leukocyte GM-CSF receptor (CD116) expression and function in inflammatory bowel disease. Gastroenterology 141: 208-216.
39. Uchida, K., D. C. Beck, T. Yamamoto, P. Y. Berclaz, S. Abe, M. K. Staudt, B. C. Carey, M. D. Filippi, S. E. Wert, L. A. Denson, et al. 2007. GM-CSF autoantibodies and neutrophil dysfunction in pulmonary alveolar proteinosis. N. Engl. J. Med. 356: 567-579.
40. Han, X., K. Uchida, I. Jurickova, D. Koch, T. Willson, C. Samson, E. Bonkowski, A. Trauernicht, M. O. Kim, G. Tomer, et al. 2009. Granulocyte-macrophage colony-stimulating factor autoantibodies in murine ileitis and progressive ileal Crohn's disease. Gastroenterology 136: 1261-1271, e1-3.
41. Dieckgraefe, B. K., and J. R. Korzenik. 2002. Treatment of active Crohn's disease with recombinant human granulocyte-macrophage colony-stimulating factor. Lancet 360: 1478-1480.
42. Korzenik, J. R., B. K. Dieckgraefe, J. F. Valentine, D. F. Hausman, and M. J. Gilbert; Sargramostim in Crohn's Disease Study Group. 2005. Sargramostim for active Crohn's disease. N. Engl. J. Med. 352: 2193-2201.
43. Valentine, J. F., R. N. Fedorak, B. Feagan, P. Fredlund, R. Schmitt, P. Ni, and T. J. Humphries. 2009. Steroid-sparing properties of sargramostim in patients with corticosteroid-dependent Crohn's disease: a randomised, double-blind, placebo-controlled, phase 2 study. Gut 58: 1354-1362.