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The Journal of Immunology, 2001, 166: 678-689.
Copyright © 2001 by The American Association of Immunologists

Increased Production of Immature Myeloid Cells in Cancer Patients: A Mechanism of Immunosuppression in Cancer1

Bond Almand*, Joseph I. Clark{dagger}, Ekaterina Nikitina2,{dagger}, James van Beynen{dagger}, Nicholas R. English{ddagger}, Stella C. Knight{ddagger}, David P. Carbone* and Dmitry I. Gabrilovich2,3,{dagger}

* Department of Medicine and The Vanderbilt Cancer Center, Vanderbilt University Medical Center, Nashville, TN 37232; {dagger} Cardinal Bernardin Cancer Center, Loyola University Medical Center, Maywood, IL 60153; and {ddagger} Imperial College School of Medicine, Northwick Park Institute for Medical Research, Harrow, United Kingdom

Defective dendritic cell (DC) function caused by abnormal differentiation of these cells is an important mechanism of tumor escape from immune system control. Previously, we have demonstrated that the number and function of DC were dramatically reduced in cancer patients. This effect was closely associated with accumulation of immature cells (ImC) in peripheral blood. In this study, we investigated the nature and functional role of those ImC. Using flow cytometry, electron microscopy, colony formation assays, and cell differentiation in the presence of different cell growth factors, we have determined that the population of ImC is composed of a small percentage (<2%) of hemopoietic progenitor cells, with all other cells being represented by MHC class I-positive myeloid cells. About one-third of ImC were immature macrophages and DC, and the remaining cells were immature myeloid cells at earlier stages of differentiation. These cells were differentiated into mature DC in the presence of 1 µM all-trans-retinoic acid. Removal of ImC from DC fractions completely restored the ability of the DC to stimulate allogeneic T cells. In two different experimental systems ImC inhibited Ag-specific T cell responses. Thus, immature myeloid cells generated in large numbers in cancer patients are able to directly inhibit Ag-specific T cell responses. This may represent a new mechanism of immune suppression in cancer and may suggest a new approach to cancer treatment.




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Gemcitabine Selectively Eliminates Splenic Gr-1+/CD11b+ Myeloid Suppressor Cells in Tumor-Bearing Animals and Enhances Antitumor Immune Activity
Clin. Cancer Res., September 15, 2005; 11(18): 6713 - 6721.
[Abstract] [Full Text] [PDF]


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BloodHome page
C. Fauriat, A. Moretta, D. Olive, and R. T. Costello
Defective killing of dendritic cells by autologous natural killer cells from acute myeloid leukemia patients
Blood, September 15, 2005; 106(6): 2186 - 2188.
[Abstract] [Full Text] [PDF]


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JCOHome page
D. P. Carbone, I. F. Ciernik, M. J. Kelley, M. C. Smith, S. Nadaf, D. Kavanaugh, V. E. Maher, M. Stipanov, D. Contois, B. E. Johnson, et al.
Immunization With Mutant p53- and K-ras-Derived Peptides in Cancer Patients: Immune Response and Clinical Outcome
J. Clin. Oncol., August 1, 2005; 23(22): 5099 - 5107.
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J. Immunol.Home page
A. Rughetti, I. Pellicciotta, M. Biffoni, M. Backstrom, T. Link, E. P. Bennet, H. Clausen, T. Noll, G. C. Hansson, J. M. Burchell, et al.
Recombinant Tumor-Associated MUC1 Glycoprotein Impairs the Differentiation and Function of Dendritic Cells
J. Immunol., June 15, 2005; 174(12): 7764 - 7772.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
A. Takahashi, M. G. V. Hanson, H. R. Norell, A. M. Havelka, K. Kono, K.-J. Malmberg, and R. V. R. Kiessling
Preferential Cell Death of CD8+ Effector Memory (CCR7-CD45RA-) T Cells by Hydrogen Peroxide-Induced Oxidative Stress
J. Immunol., May 15, 2005; 174(10): 6080 - 6087.
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Proc. Natl. Acad. Sci. USAHome page
C. De Santo, P. Serafini, I. Marigo, L. Dolcetti, M. Bolla, P. Del Soldato, C. Melani, C. Guiducci, M. P. Colombo, M. Iezzi, et al.
Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination
PNAS, March 15, 2005; 102(11): 4185 - 4190.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
P. Sinha, V. K. Clements, and S. Ostrand-Rosenberg
Reduction of Myeloid-Derived Suppressor Cells and Induction of M1 Macrophages Facilitate the Rejection of Established Metastatic Disease
J. Immunol., January 15, 2005; 174(2): 636 - 645.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. M. Dikov, J. E. Ohm, N. Ray, E. E. Tchekneva, J. Burlison, D. Moghanaki, S. Nadaf, and D. P. Carbone
Differential Roles of Vascular Endothelial Growth Factor Receptors 1 and 2 in Dendritic Cell Differentiation
J. Immunol., January 1, 2005; 174(1): 215 - 222.
[Abstract] [Full Text] [PDF]


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Am. J. Pathol.Home page
G. Gerlini, A. Tun-Kyi, C. Dudli, G. Burg, N. Pimpinelli, and F. O. Nestle
Metastatic Melanoma Secreted IL-10 Down-Regulates CD1 Molecules on Dendritic Cells in Metastatic Tumor Lesions
Am. J. Pathol., December 1, 2004; 165(6): 1853 - 1863.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
S. Beckebaum, X. Zhang, X. Chen, Z. Yu, A. Frilling, G. Dworacki, H. Grosse-Wilde, C. E. Broelsch, G. Gerken, and V. R. Cicinnati
Increased Levels of Interleukin-10 in Serum from Patients with Hepatocellular Carcinoma Correlate with Profound Numerical Deficiencies and Immature Phenotype of Circulating Dendritic Cell Subsets
Clin. Cancer Res., November 1, 2004; 10(21): 7260 - 7269.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
B. Bonnotte, M. Crittenden, N. Larmonier, M. Gough, and R. G. Vile
MIP-3{alpha} Transfection into a Rodent Tumor Cell Line Increases Intratumoral Dendritic Cell Infiltration but Enhances (Facilitates) Tumor Growth and Decreases Immunogenicity
J. Immunol., October 15, 2004; 173(8): 4929 - 4935.
[Abstract] [Full Text] [PDF]


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J. Nutr.Home page
L. M. Hengesbach and K. A. Hoag
Physiological Concentrations of Retinoic Acid Favor Myeloid Dendritic Cell Development over Granulocyte Development in Cultures of Bone Marrow Cells from Mice
J. Nutr., October 1, 2004; 134(10): 2653 - 2659.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
M. J. Skeen, M. M. Freeman, and H. K. Ziegler
Changes in peritoneal myeloid populations and their proinflammatory cytokine expression during infection with Listeria monocytogenes are altered in the absence of {gamma}/{delta} T cells
J. Leukoc. Biol., July 1, 2004; 76(1): 104 - 115.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
P. Monti, B. E. Leone, A. Zerbi, G. Balzano, S. Cainarca, V. Sordi, M. Pontillo, A. Mercalli, V. Di Carlo, P. Allavena, et al.
Tumor-Derived MUC1 Mucins Interact with Differentiating Monocytes and Induce IL-10highIL-12low Regulatory Dendritic Cell
J. Immunol., June 15, 2004; 172(12): 7341 - 7349.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
E. A. Danna, P. Sinha, M. Gilbert, V. K. Clements, B. A. Pulaski, and S. Ostrand-Rosenberg
Surgical Removal of Primary Tumor Reverses Tumor-Induced Immunosuppression Despite the Presence of Metastatic Disease
Cancer Res., March 15, 2004; 64(6): 2205 - 2211.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
Q. Li, P.-Y. Pan, P. Gu, D. Xu, and S.-H. Chen
Role of Immature Myeloid Gr-1+ Cells in the Development of Antitumor Immunity
Cancer Res., February 1, 2004; 64(3): 1130 - 1139.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
S. Kusmartsev, Y. Nefedova, D. Yoder, and D. I. Gabrilovich
Antigen-Specific Inhibition of CD8+ T Cell Response by Immature Myeloid Cells in Cancer Is Mediated by Reactive Oxygen Species
J. Immunol., January 15, 2004; 172(2): 989 - 999.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
Y. Nefedova, M. Huang, S. Kusmartsev, R. Bhattacharya, P. Cheng, R. Salup, R. Jove, and D. Gabrilovich
Hyperactivation of STAT3 Is Involved in Abnormal Differentiation of Dendritic Cells in Cancer
J. Immunol., January 1, 2004; 172(1): 464 - 474.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
V. Pisarev, B. Yu, R. Salup, S. Sherman, D. C. Altieri, and D. I. Gabrilovich
Full-Length Dominant-Negative Survivin for Cancer Immunotherapy
Clin. Cancer Res., December 15, 2003; 9(17): 6523 - 6533.
[Abstract] [Full Text] [PDF]


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BloodHome page
C. Melani, C. Chiodoni, G. Forni, and M. P. Colombo
Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity
Blood, September 15, 2003; 102(6): 2138 - 2145.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
S. Kusmartsev, F. Cheng, B. Yu, Y. Nefedova, E. Sotomayor, R. Lush, and D. Gabrilovich
All-trans-Retinoic Acid Eliminates Immature Myeloid Cells from Tumor-bearing Mice and Improves the Effect of Vaccination
Cancer Res., August 1, 2003; 63(15): 4441 - 4449.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
S. Kusmartsev and D. I. Gabrilovich
Inhibition of myeloid cell differentiation in cancer: the role of reactive oxygen species
J. Leukoc. Biol., August 1, 2003; 74(2): 186 - 196.
[Abstract] [Full Text] [PDF]


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BloodHome page
A. D. Billiau, S. Fevery, O. Rutgeerts, W. Landuyt, and M. Waer
Transient expansion of Mac1+Ly6-G+Ly6-C+ early myeloid cells with suppressor activity in spleens of murine radiation marrow chimeras: possible implications for the graft-versus-host and graft-versus-leukemia reactivity of donor lymphocyte infusions
Blood, July 15, 2003; 102(2): 740 - 748.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
Y. Liu, J. A. Van Ginderachter, L. Brys, P. De Baetselier, G. Raes, and A. B. Geldhof
Nitric Oxide-Independent CTL Suppression during Tumor Progression: Association with Arginase-Producing (M2) Myeloid Cells
J. Immunol., May 15, 2003; 170(10): 5064 - 5074.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
P. Kleindienst and T. Brocker
Endogenous Dendritic Cells Are Required for Amplification of T Cell Responses Induced by Dendritic Cell Vaccines In Vivo
J. Immunol., March 15, 2003; 170(6): 2817 - 2823.
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J. Immunol.Home page
V. Bronte, P. Serafini, C. De Santo, I. Marigo, V. Tosello, A. Mazzoni, D. M. Segal, C. Staib, M. Lowel, G. Sutter, et al.
IL-4-Induced Arginase 1 Suppresses Alloreactive T Cells in Tumor-Bearing Mice
J. Immunol., January 1, 2003; 170(1): 270 - 278.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
B. Wirleitner, D. Reider, S. Ebner, G. Bock, B. Widner, M. Jaeger, H. Schennach, N. Romani, and D. Fuchs
Monocyte-derived dendritic cells release neopterin
J. Leukoc. Biol., December 1, 2002; 72(6): 1148 - 1153.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
D. I. Gabrilovich, P. Cheng, Y. Fan, B. Yu, E. Nikitina, A. Sirotkin, M. Shurin, T. Oyama, Y. Adachi, S. Nadaf, et al.
H1{degrees} histone and differentiation of dendritic cells. A molecular target for tumor-derived factors
J. Leukoc. Biol., August 1, 2002; 72(2): 285 - 296.
[Abstract] [Full Text] [PDF]


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Molecular Cancer TherapeuticsHome page
K. Mashino, N. Sadanaga, F. Tanaka, M. Ohta, H. Yamaguchi, and M. Mori
Effective Strategy of Dendritic Cell-based Immunotherapy for Advanced Tumor-bearing Hosts: the Critical Role of Th1-dominant Immunity
Mol. Cancer Ther., August 1, 2002; 1(10): 785 - 794.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
T. K. Hoffmann, J. Muller-Berghaus, R. L. Ferris, J. T. Johnson, W. J. Storkus, and T. L. Whiteside
Alterations in the Frequency of Dendritic Cell Subsets in the Peripheral Circulation of Patients with Squamous Cell Carcinomas of the Head and Neck
Clin. Cancer Res., June 1, 2002; 8(6): 1787 - 1793.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
C. C. Sombroek, A. G. M. Stam, A. J. Masterson, S. M. Lougheed, M. J. A. G. Schakel, C. J. L. M. Meijer, H. M. Pinedo, A. J. M. van den Eertwegh, R. J. Scheper, and T. D. de Gruijl
Prostanoids Play a Major Role in the Primary Tumor-Induced Inhibition of Dendritic Cell Differentiation
J. Immunol., May 1, 2002; 168(9): 4333 - 4343.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
A. Mazzoni, V. Bronte, A. Visintin, J. H. Spitzer, E. Apolloni, P. Serafini, P. Zanovello, and D. M. Segal
Myeloid Suppressor Lines Inhibit T Cell Responses by an NO-Dependent Mechanism
J. Immunol., January 15, 2002; 168(2): 689 - 695.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
D. I. Gabrilovich, M. P. Velders, E. M. Sotomayor, and W. M. Kast
Mechanism of Immune Dysfunction in Cancer Mediated by Immature Gr-1+ Myeloid Cells
J. Immunol., May 1, 2001; 166(9): 5398 - 5406.
[Abstract] [Full Text] [PDF]




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