Dysregulated Hematopoietic Stem and Progenitor Cell Activity Promotes Interleukin-23-Driven Chronic Intestinal Inflammation

被引:163
作者
Griseri, Thibault [1 ]
McKenzie, Brent S. [2 ]
Schiering, Chris [1 ]
Powrie, Fiona [1 ,3 ]
机构
[1] Univ Oxford, John Radcliffe Hosp, Nuffield Dept Clin Med, Translat Gastroenterol Unit,Expt Med Div, Oxford OX3 9DU, England
[2] Univ Melbourne, Mol Sci & Biotechnol Inst Bio21, CSL Ltd, Res Dept, Parkville, Vic 3010, Australia
[3] Univ Oxford, Sir William Dunn Sch Pathol, Oxford OX1 3RE, England
基金
英国惠康基金;
关键词
COLONY-STIMULATING FACTOR; T-CELLS; IFN-GAMMA; DISEASE; INNATE; IDENTIFICATION; PROLIFERATION; EXPRESSION; RECEPTORS; BLOOD;
D O I
10.1016/j.immuni.2012.08.025
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
In interleukin-23 (IL-23)-dependent colitis, there is excessive accumulation of short-lived neutrophils and inflammatory monocytes in the intestine. It is unknown whether this reflects changes in mature cell populations or whether the IL-23-driven colitogenic T cell program regulates upstream hematopoietic stem and progenitor cells (HSPC). Here we have shown dysregulation of hematopoiesis in colitis mediated by inflammatory cytokines. First, there was an interferon-gamma-dependent accumulation of proliferating hematopoietic stem cells in the bone marrow and spleen. Second, there was a strong skew toward granulocyte-monocyte progenitor (GMP) production at the expense of erythroid and lymphoid progenitors. Extramedullary hematopoiesis was also evident, and granulocyte macrophage-colony stimulating factor (GM-CSF) blockade reduced the accumulation of splenic and colonic GMPs, resulting in amelioration of colitis. Importantly, transfer of GMPs exacerbated colitis. These data identify HSPCs as a major target of the IL-23-driven inflammatory axis suggesting therapeutic strategies for the treatment of inflammatory bowel disease.
引用
收藏
页码:1116 / 1129
页数:14
相关论文
共 41 条
[1]   Interleukin-23 Drives Intestinal Inflammation through Direct Activity on T Cells [J].
Ahern, Philip P. ;
Schiering, Chris ;
Buonocore, Sofia ;
McGeachy, Mandy J. ;
Cua, Dan J. ;
Maloy, Kevin J. ;
Powrie, Fiona .
IMMUNITY, 2010, 33 (02) :279-288
[2]   A clonogenic common myeloid progenitor that gives rise to all myeloid lineages [J].
Akashi, K ;
Traver, D ;
Miyamoto, T ;
Weissman, IL .
NATURE, 2000, 404 (6774) :193-197
[3]   Quiescent haematopoietic stem cells are activated by IFN-γ in response to chronic infection [J].
Baldridge, Megan T. ;
King, Katherine Y. ;
Boles, Nathan C. ;
Weksberg, David C. ;
Goodell, Margaret A. .
NATURE, 2010, 465 (7299) :793-U9
[4]   Induction of an IL7-R+c-Kithi myelolymphoid progenitor critically dependent on IFN-γ signaling during acute malaria [J].
Belyaev, Nikolai N. ;
Brown, Douglas E. ;
Diaz, Ana-Isabel Garcia ;
Rae, Aaron ;
Jarra, William ;
Thompson, Joanne ;
Langhorne, Jean ;
Potocnik, Alexandre J. .
NATURE IMMUNOLOGY, 2010, 11 (06) :477-U41
[5]   Niche recycling through division-independent egress of hematopoietic stem cells [J].
Bhattacharya, Deepta ;
Czechowicz, Agnieszka ;
Ooi, A. G. Lisa ;
Rossi, Derrick J. ;
Bryder, David ;
Weissman, Irving L. .
JOURNAL OF EXPERIMENTAL MEDICINE, 2009, 206 (12) :2837-2850
[6]   Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology [J].
Buonocore, Sofia ;
Ahern, Philip P. ;
Uhlig, Holm H. ;
Ivanov, Ivaylo I. ;
Littman, Dan R. ;
Maloy, Kevin J. ;
Powrie, Fiona .
NATURE, 2010, 464 (7293) :1371-1375
[7]   Mammalian target of rapamycin activation underlies HSC defects in autoimmune disease and inflammation in mice [J].
Chen, Chong ;
Liu, Yu ;
Liu, Yang ;
Zheng, Pan .
JOURNAL OF CLINICAL INVESTIGATION, 2010, 120 (11) :4091-4101
[8]   Neutrophil transepithelial migration and epithelial barrier function in IBD - Potential targets for inhibiting neutrophil trafficking [J].
Chin, Alex C. ;
Parkos, Charles A. .
INFLAMMATORY BOWEL DISEASE: GENETICS, BARRIER FUNCTION, IMMUNOLOGIC MECHANISMS, AND MICROBIAL PATHWAYS, 2006, 1072 :276-287
[9]   RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation [J].
Codarri, Laura ;
Gyuelveszi, Gabor ;
Tosevski, Vinko ;
Hesske, Lysann ;
Fontana, Adriano ;
Magnenat, Laurent ;
Suter, Tobias ;
Becher, Burkhard .
NATURE IMMUNOLOGY, 2011, 12 (06) :560-U248
[10]   The encephalitogenicity of TH17 cells is dependent on IL-1-and IL-23-induced production of the cytokine GM-CSF [J].
El-Behi, Mohamed ;
Ciric, Bogoljub ;
Dai, Hong ;
Yan, Yaping ;
Cullimore, Melissa ;
Safavi, Farinaz ;
Zhang, Guang-Xian ;
Dittel, Bonnie N. ;
Rostami, Abdolmohamad .
NATURE IMMUNOLOGY, 2011, 12 (06) :568-U241