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The Journal of Immunology, 2000, 164: 6166-6173.
Copyright © 2000 by The American Association of Immunologists

M-1/M-2 Macrophages and the Th1/Th2 Paradigm1

Charles D. Mills2, Kristi Kincaid, Jennifer M. Alt, Michelle J. Heilman and Annette M. Hill

Department of Surgery, University of Minnesota, Minneapolis, MN 55455

Evidence is provided that macrophages can make M-1 or M-2 responses. The concept of M-1/M-2 fomented from observations that macrophages from prototypical Th1 strains (C57BL/6, B10D2) are more easily activated to produce NO with either IFN-{gamma} or LPS than macrophages from Th2 strains (BALB/c, DBA/2). In marked contrast, LPS stimulates Th2, but not Th1, macrophages to increase arginine metabolism to ornithine. Thus, M-1/M-2 does not simply describe activated or unactivated macrophages, but cells expressing distinct metabolic programs. Because NO inhibits cell division, while ornithine can stimulate cell division (via polyamines), these results also indicate that M-1 and M-2 responses can influence inflammatory reactions in opposite ways. Macrophage TGF-ß1, which inhibits inducible NO synthase and stimulates arginase, appears to play an important role in regulating the balance between M-1 and M-2. M-1/M-2 phenotypes are independent of T or B lymphocytes because C57BL/6 and BALB/c NUDE or SCID macrophages also exhibit M-1/M-2. Indeed, M-1/M-2 proclivities are magnified in NUDE and SCID mice. Finally, C57BL/6 SCID macrophages cause CB6F1 lymphocytes to increase IFN-{gamma} production, while BALB/c SCID macrophages increase TGF-ß production. Together, the results indicate that M-1- or M-2-dominant macrophage responses can influence whether Th1/Th2 or other types of inflammatory responses occur.




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Mouse Strain Susceptibility to Trypanosome Infection: An Arginase-Dependent Effect
J. Immunol., May 15, 2004; 172(10): 6298 - 6303.
[Abstract] [Full Text] [PDF]


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Exp. Biol. Med.Home page
A. T. Borchers, C. L. Keen, and M. E. Gershwin
Mushrooms, Tumors, and Immunity: An Update
Experimental Biology and Medicine, May 1, 2004; 229(5): 393 - 406.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
A. E. Oran and H. L. Robinson
DNA Vaccines: Influenza Virus Challenge of a Th2/Tc2 Immune Response Results in a Th2/Tc1 Response in the Lung
J. Virol., April 15, 2004; 78(8): 4376 - 4380.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
L. C. Gavrilescu, B. A. Butcher, L. Del Rio, G. A. Taylor, and E. Y. Denkers
STAT1 Is Essential for Antimicrobial Effector Function but Dispensable for Gamma Interferon Production during Toxoplasma gondii Infection
Infect. Immun., March 1, 2004; 72(3): 1257 - 1264.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
T. H. Wu, C. N. Pabin, Z. Qin, T. Blankenstein, M. Philip, J. Dignam, K. Schreiber, and H. Schreiber
Long-Term Suppression of Tumor Growth by TNF Requires a Stat1- and IFN Regulatory Factor 1-Dependent IFN-{gamma} Pathway but Not IL-12 or IL-18
J. Immunol., March 1, 2004; 172(5): 3243 - 3251.
[Abstract] [Full Text] [PDF]


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IOVSHome page
J. Yamada, K. Maruyama, Y. Sano, S. Kinoshita, Y. Murata, and J. Hamuro
Promotion of Corneal Allograft Survival by the Induction of Oxidative Macrophages
Invest. Ophthalmol. Vis. Sci., February 1, 2004; 45(2): 448 - 454.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
T. Katakura, M. Miyazaki, M. Kobayashi, D. N. Herndon, and F. Suzuki
CCL17 and IL-10 as Effectors That Enable Alternatively Activated Macrophages to Inhibit the Generation of Classically Activated Macrophages
J. Immunol., February 1, 2004; 172(3): 1407 - 1413.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
D. H. Dockrell, H. M. Marriott, L. R. Prince, V. C. Ridger, P. G. Ince, P. G. Hellewell, and M. K. B. Whyte
Alveolar Macrophage Apoptosis Contributes to Pneumococcal Clearance in a Resolving Model of Pulmonary Infection
J. Immunol., November 15, 2003; 171(10): 5380 - 5388.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
H. Wang, K. A. Hosiawa, W. Min, J. Yang, X. Zhang, B. Garcia, T. E. Ichim, D. Zhou, D. Lian, D. J. Kelvin, et al.
Cytokines Regulate the Pattern of Rejection and Susceptibility to Cyclosporine Therapy in Different Mouse Recipient Strains After Cardiac Allografting
J. Immunol., October 1, 2003; 171(7): 3823 - 3836.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
A. C. La Flamme, K. Ruddenklau, and B. T. Backstrom
Schistosomiasis Decreases Central Nervous System Inflammation and Alters the Progression of Experimental Autoimmune Encephalomyelitis
Infect. Immun., September 1, 2003; 71(9): 4996 - 5004.
[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
S. A. McClellan, X. Huang, R. P. Barrett, N. van Rooijen, and L. D. Hazlett
Macrophages Restrict Pseudomonas aeruginosa Growth, Regulate Polymorphonuclear Neutrophil Influx, and Balance Pro- and Anti-Inflammatory Cytokines in BALB/c Mice
J. Immunol., May 15, 2003; 170(10): 5219 - 5227.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
D. M. Mosser
The many faces of macrophage activation
J. Leukoc. Biol., February 1, 2003; 73(2): 209 - 212.
[Full Text] [PDF]


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ThoraxHome page
F L M Ricciardolo
Multiple roles of nitric oxide in the airways
Thorax, February 1, 2003; 58(2): 175 - 182.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
E. Kuroda and U. Yamashita
Mechanisms of Enhanced Macrophage-Mediated Prostaglandin E2 Production and Its Suppressive Role in Th1 Activation in Th2-Dominant BALB/c Mice
J. Immunol., January 15, 2003; 170(2): 757 - 764.
[Abstract] [Full Text] [PDF]


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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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BloodHome page
A. B. Geldhof, J. A. Van Ginderachter, Y. Liu, W. Noel, G. Raes, and P. De Baetselier
Antagonistic effect of NK cells on alternatively activated monocytes: a contribution of NK cells to CTL generation
Blood, December 1, 2002; 100(12): 4049 - 4058.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
W. Noel, G. Hassanzadeh, G. Raes, B. Namangala, I. Daems, L. Brys, F. Brombacher, P. D. Baetselier, and A. Beschin
Infection Stage-Dependent Modulation of Macrophage Activation in Trypanosoma congolense-Resistant and -Susceptible Mice
Infect. Immun., November 1, 2002; 70(11): 6180 - 6187.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
J. S. Welch, L. Escoubet-Lozach, D. B. Sykes, K. Liddiard, D. R. Greaves, and C. K. Glass
TH2 Cytokines and Allergic Challenge Induce Ym1 Expression in Macrophages by a STAT6-dependent Mechanism
J. Biol. Chem., November 1, 2002; 277(45): 42821 - 42829.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
D. A. Hume, I. L. Ross, S. R. Himes, R. T. Sasmono, C. A. Wells, and T. Ravasi
The mononuclear phagocyte system revisited
J. Leukoc. Biol., October 1, 2002; 72(4): 621 - 627.
[Abstract] [Full Text] [PDF]


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Am. J. Respir. Cell Mol. Bio.Home page
E. M. Janssen, M. H. M. Wauben, F. P. Nijkamp, W. van Eden, and A. J. M. van Oosterhout
Immunomodulatory Effects of Antigen-Pulsed Macrophages in a Murine Model of Allergic Asthma
Am. J. Respir. Cell Mol. Biol., August 1, 2002; 27(2): 257 - 264.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
E. Kuroda, T. Kito, and U. Yamashita
Reduced Expression of STAT4 and IFN-{gamma} in Macrophages from BALB/c Mice
J. Immunol., June 1, 2002; 168(11): 5477 - 5482.
[Abstract] [Full Text] [PDF]


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Am. J. Respir. Cell Mol. Bio.Home page
E. Careau, J. Sirois, and E. Y. Bissonnette
Characterization of Lung Hyperresponsiveness, Inflammation, and Alveolar Macrophage Mediator Production in Allergy Resistant and Susceptible Rats
Am. J. Respir. Cell Mol. Biol., May 1, 2002; 26(5): 579 - 586.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
L. Tuckova, J. Novotna, P. Novak, Z. Flegelova, T. Kveton, L. Jelinkova, Z. Zidek, P. Man, and H. Tlaskalova-Hogenova
Activation of macrophages by gliadin fragments: isolation and characterization of active peptide
J. Leukoc. Biol., April 1, 2002; 71(4): 625 - 631.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
J. Huang, F. J. DeGraves, S. D. Lenz, D. Gao, P. Feng, D. Li, T. Schlapp, and B. Kaltenboeck
The quantity of nitric oxide released by macrophages regulates Chlamydia-induced disease
PNAS, March 19, 2002; 99(6): 3914 - 3919.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
K. R. B. Bastos, J. M. Alvarez, C. R. F. Marinho, L. V. Rizzo, and M. R. D'Imperio Lima
Macrophages from IL-12p40-deficient mice have a bias toward the M2 activation profile
J. Leukoc. Biol., February 1, 2002; 71(2): 271 - 278.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
T. Ravasi, C. Wells, A. Forest, D. M. Underhill, B. J. Wainwright, A. Aderem, S. Grimmond, and D. A. Hume
Generation of Diversity in the Innate Immune System: Macrophage Heterogeneity Arises from Gene-Autonomous Transcriptional Probability of Individual Inducible Genes
J. Immunol., January 1, 2002; 168(1): 44 - 50.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. Hesse, M. Modolell, A. C. La Flamme, M. Schito, J. M. Fuentes, A. W. Cheever, E. J. Pearce, and T. A. Wynn
Differential Regulation of Nitric Oxide Synthase-2 and Arginase-1 by Type 1/Type 2 Cytokines In Vivo: Granulomatous Pathology Is Shaped by the Pattern of L-Arginine Metabolism
J. Immunol., December 1, 2001; 167(11): 6533 - 6544.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
S.-H. Su, H.-i. Chen, and C. J. Jen
C57BL/6 and BALB/c Bronchoalveolar Macrophages Respond Differently to Exercise
J. Immunol., November 1, 2001; 167(9): 5084 - 5091.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
F.-D. Shi, M. Flodstrom, S. H. Kim, S. Pakala, M. Cleary, H.-G. Ljunggren, and N. Sarvetnick
Control of the Autoimmune Response by Type 2 Nitric Oxide Synthase
J. Immunol., September 1, 2001; 167(5): 3000 - 3006.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
A. S. MacDonald, A. D. Straw, B. Bauman, and E. J. Pearce
CD8- Dendritic Cell Activation Status Plays an Integral Role in Influencing Th2 Response Development
J. Immunol., August 15, 2001; 167(4): 1982 - 1988.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
L. C. Gavrilescu and E. Y. Denkers
IFN-{{gamma}} Overproduction and High Level Apoptosis Are Associated with High but Not Low Virulence Toxoplasma gondii Infection
J. Immunol., July 15, 2001; 167(2): 902 - 909.
[Abstract] [Full Text] [PDF]


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IOVSHome page
J. Hori and J. W. Streilein
Dynamics of Donor Cell Persistence and Recipient Cell Replacement in Orthotopic Corneal Allografts in Mice
Invest. Ophthalmol. Vis. Sci., July 1, 2001; 42(8): 1820 - 1828.
[Abstract] [Full Text] [PDF]


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JEMHome page
V. Iniesta, L. C. Gomez-Nieto, and I. Corraliza
The Inhibition of Arginase by N{omega}-Hydroxy-L-Arginine Controls the Growth of Leishmania Inside Macrophages
J. Exp. Med., March 19, 2001; 193(6): 777 - 784.
[Abstract] [Full Text] [PDF]




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