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Blood, 15 April 2005, Vol. 105, No. 8, pp. 3011-3018.
Prepublished online as a Blood First Edition Paper on December 16, 2004; DOI 10.1182/blood-2004-10-4072.
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PLENARY PAPERS
Differential expression of SHIP1 in CD56bright and CD56dim NK cells provides a molecular basis for distinct functional responses to monokine costimulation
Rossana Trotta,
Robin Parihar,
Jianhua Yu,
Brian Becknell,
Jeffrey Allard, II,
Jing Wen,
Wei Ding,
Hsiaoyin Mao,
Susheela Tridandapani,
William E. Carson, and
Michael A. Caligiuri
From the Division of Human Cancer Genetics, Department of Molecular Virology, Immunology, and Medical Genetics; Medical Scientific Program, Integrated Biomedical Graduate Program, College of Medicine and Public Health; Division of Pulmonary and Critical Care, Department of Internal Medicine; The Comprehensive Cancer Center, The Ohio State University; Division of Surgical Oncology, Department of Surgery; and Division of Hematology/Oncology, Department of Internal Medicine, The Ohio State University, Columbus, OH.
Monocyte cytokines (ie, monokines) induce natural killer (NK) cells to produce interferon- (IFN-), which is critical for monocyte clearance of infectious pathogens and tumor surveillance. Human CD56bright NK cells produce far more IFN- in response to monokines than do CD56dim NK cells. The kinases and phosphatases involved in regulating IFN- production by monokine-activated NK cells are not clearly identified. SHIP1 is a 5' inositol phosphatase that dephosphorylates the phosphatidylinositol-3 kinase (PI-3K) product PI3,4,5P3. Here, we show that constitutive expression of SHIP1 is distinctly lower in CD56bright NK cells compared with CD56dim NK cells, suggesting it could be an important negative regulator of IFN- production in monokine-activated NK cells. Indeed, overexpression of SHIP1 in CD56bright NK cells followed by monokine activation substantially lowered IFN- production. This effect was not seen when NK cells were infected with a SHIP1 mutant containing an inactive catalytic domain. Finally, NK cells in SHIP1–/– mice produced more IFN- in response to monokines in vivo than did NK cells from wild-type mice. Collectively, these results demonstrate that SHIP1 negatively regulates monokine-induced NK cell IFN- production in vitro and in vivo and provide the first molecular explanation for an important functional distinction observed between CD56bright and CD56dim human NK subsets.
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