Galectin-3 facilitates neutrophil recruitment as an innate immune response to a parasitic protozoa cutaneous infection

Journal of Immunology

Volumn 190, Issue 2, 2013, Pages 630-640

  Bhaumik, Pampa ^a   St Pierre, Guillaume ^a   Milot, Valérie ^a   St Pierre, Christian ^a   Sato, Sachiko ^a  

^a Faculty of Medicine   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GALECTIN 3; MYELOPEROXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PHAGOCYTOSIS; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVITY; ENZYME ASSAY; HOST RESISTANCE; INFECTION CONTROL; LEUKOCYTE FUNCTION; LEUKOCYTE MIGRATION; MOLECULAR BIOLOGY; MOUSE; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL RECRUITMENT; NONHUMAN; PARASITE LOAD; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN ANALYSIS; PROTEIN SECRETION; SKIN LEISHMANIASIS; WESTERN BLOTTING; WILD TYPE;

ANIMALS; CELL MOVEMENT; CYTOKINES; DISEASE MODELS, ANIMAL; GALECTIN 3; IMMUNITY, INNATE; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; LYMPH NODES; MICE; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION;

EID: 84872177718     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103197     Document Type: Article

References (101)

1. Segal, A. W. 2005. How neutrophils kill microbes. Annu. Rev. Immunol. 23: 197-223.
2. Nathan, C. 2006. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6: 173-182.
3. Soehnlein, O. 2009. An elegant defense: how neutrophils shape the immune response. Trends Immunol. 30: 511-512.
4. Borregaard, N., and J. B. Cowland. 1997. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood 89: 3503-3521.
5. Papayannopoulos, V., and A. Zychlinsky. 2009. NETs: a new strategy for using old weapons. Trends Immunol. 30: 513-521.
6. Gabriel, C., W. R. McMaster, D. Girard, and A. Descoteaux. 2010. Leishmania donovani promastigotes evade the antimicrobial activity of neutrophil extracellular traps. J. Immunol. 185: 4319-4327.
7. Guimarães-Costa, A. B., M. T. Nascimento, G. S. Froment, R. P. Soares, F. N. Morgado, F. Conceição-Silva, and E. M. Saraiva. 2009. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc. Natl. Acad. Sci. USA 106: 6748-6753.
8. Tuomanen, E. I., R. Austrian, and H. R. Masure. 1995. Pathogenesis of pneumococcal infection. N. Engl. J. Med. 332: 1280-1284.
9. Abraham, E. 2003. Neutrophils and acute lung injury. Crit. Care Med. 31 (Suppl. 4): S195-S199.
10. Hogg, J. C., and C. M. Doerschuk. 1995. Leukocyte traffic in the lung. Annu. Rev. Physiol. 57: 97-114.
11. Butcher, E. C., and L. J. Picker. 1996. Lymphocyte homing and homeostasis. Science 272: 60-66.
12. Carlos, T. M., and J. M. Harlan. 1994. Leukocyte-endothelial adhesion molecules. Blood 84: 2068-2101.
13. Springer, T. A. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76: 301-314.
14. Mizgerd, J. P., H. Kubo, G. J. Kutkoski, S. D. Bhagwan, K. Scharffetter-Kochanek, A. L. Beaudet, and C. M. Doerschuk. 1997. Neutrophil emigration in the skin, lungs, and peritoneum: different requirements for CD11/CD18 revealed by CD18-deficient mice. J. Exp. Med. 186: 1357-1364.
15. Mizgerd, J. P., B. H. Horwitz, H. C. Quillen, M. L. Scott, and C. M. Doerschuk. 1999. Effects of CD18 deficiency on the emigration of murine neutrophils during pneumonia. J. Immunol. 163: 995-999.
16. Doerschuk, C. M., R. K. Winn, H. O. Coxson, and J. M. Harlan. 1990. CD18-dependent and -independent mechanisms of neutrophil emigration in the pulmonary and systemic microcirculation of rabbits. J. Immunol. 144: 2327-2333.
17. Kumasaka, T., N. A. Doyle, W. M. Quinlan, L. Graham, and C. M. Doerschuk. 1996. Role of CD 11/CD 18 in neutrophil emigration during acute and recurrent Pseudomonas aeruginosa-induced pneumonia in rabbits. Am. J. Pathol. 148: 1297-1305.
18. Mizgerd, J. P., B. B. Meek, G. J. Kutkoski, D. C. Bullard, A. L. Beaudet, and C. M. Doerschuk. 1996. Selectins and neutrophil traffic: margination and Streptococcus pneumoniae-induced emigration in murine lungs. J. Exp. Med. 184: 639-645.
19. Doerschuk, C. M. 2001. Mechanisms of leukocyte sequestration in inflamed lungs. Microcirculation 8: 71-88.
20. Burns, A. R., and C. M. Doerschuk. 1994. Quantitation of L-selectin and CD18 expression on rabbit neutrophils during CD18-independent and CD18-dependent emigration in the lung. J. Immunol. 153: 3177-3188.
21. Burns, A. R., C. W. Smith, and D. C. Walker. 2003. Unique structural features that influence neutrophil emigration into the lung. Physiol. Rev. 83: 309-336.
22. Tasaka, S., S. E. Richer, J. P. Mizgerd, and C. M. Doerschuk. 2002. Very late antigen-4 in CD18-independent neutrophil emigration during acute bacterial pneumonia in mice. Am. J. Respir. Crit. Care Med. 166: 53-60.
23. Mackarel, A. J., K. J. Russell, C. M. Ryan, S. J. Hislip, J. C. Rendall, M. X. FitzGerald, and C. M. O'Connor. 2001. CD18 dependency of transendothelial neutrophil migration differs during acute pulmonary inflammation. J. Immunol. 167: 2839-2846.
24. Mackarel, A. J., B. J. Plant, M. X. FitzGerald, C. M. O'Connor, L. Martin, J. S. Elborn, and C. G. Gallagher. 2005. Cystic fibrosis sputum stimulates CD18-independent neutrophil migration across endothelial cells. Exp. Lung Res. 31: 377-390.
25. Brady, H. R. 1994. Leukocyte adhesion molecules and kidney diseases. Kidney Int. 45: 1285-1300.
26. Langdale, L. A., L. C. Flaherty, H. D. Liggitt, J. M. Harlan, C. L. Rice, and R. K. Winn. 1993. Neutrophils contribute to hepatic ischemia-reperfusion injury by a CD18-independent mechanism. J. Leukoc. Biol. 53: 511-517.
27. Entman, M. L., and C. W. Smith. 1994. Postreperfusion inflammation: a model for reaction to injury in cardiovascular disease. Cardiovasc. Res. 28: 1301-1311.
28. Winn, R. K., and J. M. Harlan. 1993. CD18-independent neutrophil and mononuclear leukocyte emigration into the peritoneum of rabbits. J. Clin. Invest. 92: 1168-1173.
29. Li, Z., A. R. Burns, and C. W. Smith. 2006. Two waves of neutrophil emigration in response to corneal epithelial abrasion: distinct adhesion molecule requirements. Invest. Ophthalmol. Vis. Sci. 47: 1947-1955.
30. Rabinovich, G. A., and M. A. Toscano. 2009. Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat. Rev. Immunol. 9: 338-352.
31. Sato, S., C. St-Pierre, P. Bhaumik, and J. Nieminen. 2009. Galectins in innate immunity: dual functions of host soluble beta-galactoside-binding lectins as damage-associated molecular patterns (DAMPs) and as receptors for pathogen-associated molecular patterns (PAMPs). Immunol. Rev. 230: 172-187.
32. Nieminen, J., C. St-Pierre, P. Bhaumik, F. Poirier, and S. Sato. 2008. Role of galectin-3 in leukocyte recruitment in a murine model of lung infection by Streptococcus pneumoniae. J. Immunol. 180: 2466-2473.
33. Sato, S., and R. C. Hughes. 1994. Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. J. Biol. Chem. 269: 4424-4430.
34. Sato, S., N. Ouellet, I. Pelletier, M. Simard, A. Rancourt, and M. G. Bergeron. 2002. Role of galectin-3 as an adhesion molecule for neutrophil extravasation during streptococcal pneumonia. J. Immunol. 168: 1813-1822.
35. Sundblad, V., D. O. Croci, and G. A. Rabinovich. 2011. Regulated expression of galectin-3, a multifunctional glycan-binding protein, in haematopoietic and non-haematopoietic tissues. Histol. Histopathol. 26: 247-265.
36. Matzinger, P., and T. Kamala. 2011. Tissue-based class control: the other side of tolerance. Nat. Rev. Immunol. 11: 221-230.
37. Sacks, D., and N. Noben-Trauth. 2002. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2: 845-858.
38. Xin, L., D. A. Vargas-Inchaustegui, S. S. Raimer, B. C. Kelly, J. Hu, L. Zhu, J. Sun, and L. Soong. 2010. Type I IFN receptor regulates neutrophil functions and innate immunity to Leishmania parasites. J. Immunol. 184: 7047-7056.
39. Beil, W. J., G. Meinardus-Hager, D. C. Neugebauer, and C. Sorg. 1992. Differences in the onset of the inflammatory response to cutaneous leishmaniasis in resistant and susceptible mice. J. Leukoc. Biol. 52: 135-142.
40. Lima, G. M., A. L. Vallochi, U. R. Silva, E. M. Bevilacqua, M. M. Kiffer, and I. A. Abrahamsohn. 1998. The role of polymorphonuclear leukocytes in the resistance to cutaneous Leishmaniasis. Immunol. Lett. 64: 145-151.
41. Peters, N. C., J. G. Egen, N. Secundino, A. Debrabant, N. Kimblin, S. Kamhawi, P. Lawyer, M. P. Fay, R. N. Germain, and D. Sacks. 2008. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321: 970-974.
42. Charmoy, M., F. Auderset, C. Allenbach, and F. Tacchini-Cottier. 2010. The prominent role of neutrophils during the initial phase of infection by Leishmania parasites. J. Biomed. Biotechnol. 2010: 719361.
43. Sacks, D., and C. Anderson. 2004. Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice. Immunol. Rev. 201: 225-238.
44. Ritter, U., F. Frischknecht, and G. van Zandbergen. 2009. Are neutrophils important host cells for Leishmania parasites? Trends Parasitol. 25: 505-510.
45. Ribeiro-Gomes, F. L., A. C. Otero, N. A. Gomes, M. C. Moniz-De-Souza, L. Cysne-Finkelstein, A. C. Arnholdt, V. L. Calich, S. G. Coutinho, M. F. Lopes, and G. A. DosReis. 2004. Macrophage interactions with neutrophils regulate Leishmania major infection. J. Immunol. 172: 4454-4462.
46. Peters, N. C., and D. L. Sacks. 2009. The impact of vector-mediated neutrophil recruitment on cutaneous leishmaniasis. Cell. Microbiol. 11: 1290-1296.
47. Tacchini-Cottier, F., T. Weinkopff, and P. Launois. 2012. Does T Helper Differentiation Correlate with Resistance or Susceptibility to Infection with L. major? Some Insights From the Murine Model. Front Immunol 3: 32.
48. Pelletier, I., T. Hashidate, T. Urashima, N. Nishi, T. Nakamura, M. Futai, Y. Arata, K. Kasai, M. Hirashima, J. Hirabayashi, and S. Sato. 2003. Specific recognition of Leishmania major poly-beta-galactosyl epitopes by galectin-9: possible implication of galectin-9 in interaction between L. major and host cells. J. Biol. Chem. 278: 22223-22230.
49. St-Pierre, C., M. Ouellet, M. J. Tremblay, and S. Sato. 2010. Galectin-1 and HIV-1 Infection. Methods Enzymol. 480: 267-294.
50. Tessier, P. A., P. H. Naccache, I. Clark-Lewis, R. P. Gladue, K. S. Neote, and S. R. McColl. 1997. Chemokine networks in vivo: involvement of C-X-C and C-C chemokines in neutrophil extravasation in vivo in response to TNF-alpha. J. Immunol. 159: 3595-3602.
51. Ryckman, C., K. Vandal, P. Rouleau, M. Talbot, and P. A. Tessier. 2003. Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J. Immunol. 170: 3233-3242.
52. Matte, C., and M. Olivier. 2002. Leishmania-induced cellular recruitment during the early inflammatory response: modulation of proinflammatory mediators. J. Infect. Dis. 185: 673-681.
53. Fillion, I., N. Ouellet, M. Simard, Y. Bergeron, S. Sato, and M. G. Bergeron. 2001. Role of chemokines and formyl peptides in pneumococcal pneumonia-induced monocyte/macrophage recruitment. J. Immunol. 166: 7353-7361.
54. Daley, J. M., A. A. Thomay, M. D. Connolly, J. S. Reichner, and J. E. Albina. 2008. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83: 64-70.
55. Basu, R., S. Bhaumik, J. M. Basu, K. Naskar, T. De, and S. Roy. 2005. Kinetoplastid membrane protein-11 DNA vaccination induces complete protection against both pentavalent antimonial-sensitive and -resistant strains of Leishmania donovani that correlates with inducible nitric oxide synthase activity and IL-4 generation: evidence for mixed Th1- and Th2-like responses in visceral leishmaniasis. J. Immunol. 174: 7160-7171.
56. Tacchini-Cottier, F., C. Zweifel, Y. Belkaid, C. Mukankundiye, M. Vasei, P. Launois, G. Milon, and J. A. Louis. 2000. An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major. J. Immunol. 165: 2628-2636.
57. Chtanova, T., M. Schaeffer, S. J. Han, G. G. van Dooren, M. Nollmann, P. Herzmark, S. W. Chan, H. Satija, K. Camfield, H. Aaron, et al. 2008. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29: 487-496.
58. Beauvillain, C., P. Cunin, A. Doni, M. Scotet, S. Jaillon, M. L. Loiry, G. Magistrelli, K. Masternak, A. Chevailler, Y. Delneste, and P. Jeannin. 2011. CCR7 is involved in the migration of neutrophils to lymph nodes. Blood 117: 1196-1204.
59. Breuilh, L., F. Vanhoutte, J. Fontaine, C. M. van Stijn, I. Tillie-Leblond, M. Capron, C. Faveeuw, T. Jouault, I. van Die, P. Gosset, and F. Trottein. 2007. Galectin-3 modulates immune and inflammatory responses during helminthic infection: impact of galectin-3 deficiency on the functions of dendritic cells. Infect. Immun. 75: 5148-5157.
60. Mantovani, A., M. A. Cassatella, C. Costantini, and S. Jaillon. 2011. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11: 519-531.
61. Soehnlein, O., and L. Lindbom. 2010. Phagocyte partnership during the onset and resolution of inflammation. Nat. Rev. Immunol. 10: 427-439.
62. Stark, M. A., Y. Huo, T. L. Burcin, M. A. Morris, T. S. Olson, and K. Ley. 2005. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22: 285-294.
63. Sano, H., D. K. Hsu, J. R. Apgar, L. Yu, B. B. Sharma, I. Kuwabara, S. Izui, and F. T. Liu. 2003. Critical role of galectin-3 in phagocytosis by macrophages. J. Clin. Invest. 112: 389-397.
64. Kiwaki, K., C. M. Novak, D. K. Hsu, F. T. Liu, and J. A. Levine. 2007. Galectin-3 stimulates preadipocyte proliferation and is up-regulated in growing adipose tissue. Obesity (Silver Spring) 15: 32-39.
65. Kubes, P., and S. M. Kerfoot. 2001. Leukocyte recruitment in the microcirculation: the rolling paradigm revisited. News Physiol. Sci. 16: 76-80.
66. Kiss, J., S. Jalkanen, F. Fülöp, T. Savunen, and M. Salmi. 2008. Ischemia-reperfusion injury is attenuated in VAP-1-deficient mice and by VAP-1 inhibitors. Eur. J. Immunol. 38: 3041-3049.
67. Jalkanen, S., and M. Salmi. 2008. VAP-1 and CD73, endothelial cell surface enzymes in leukocyte extravasation. Arterioscler. Thromb. Vasc. Biol. 28: 18-26.
68. Nieminen, J., A. Kuno, J. Hirabayashi, and S. Sato. 2007. Visualization of galectin-3 oligomerization on the surface of neutrophils and endothelial cells using fluorescence resonance energy transfer. J. Biol. Chem. 282: 1374-1383.
69. Farnworth, S. L., N. C. Henderson, A. C. Mackinnon, K. M. Atkinson, T. Wilkinson, K. Dhaliwal, K. Hayashi, A. J. Simpson, A. G. Rossi, C. Haslett, and T. Sethi. 2008. Galectin-3 reduces the severity of pneumococcal pneumonia by augmenting neutrophil function. Am. J. Pathol. 172: 395-405.
70. Wang, J., R. A. Barke, R. Charboneau, and S. Roy. 2005. Morphine impairs host innate immune response and increases susceptibility to Streptococcus pneumoniae lung infection. J. Immunol. 174: 426-434.
71. Hsu, D. K., R. Y. Yang, Z. Pan, L. Yu, D. R. Salomon, W. P. Fung-Leung, and F. T. Liu. 2000. Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses. Am. J. Pathol. 156: 1073-1083.
72. Colnot, C., M. A. Ripoche, G. Milon, X. Montagutelli, P. R. Crocker, and F. Poirier. 1998. Maintenance of granulocyte numbers during acute peritonitis is defective in galectin-3-null mutant mice. Immunology 94: 290-296.
73. Bianchi, M. E. 2007. DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol. 81: 1-5.
74. Kono, H., and K. L. Rock. 2008. How dying cells alert the immune system to danger. Nat. Rev. Immunol. 8: 279-289.
75. Rubartelli, A., and M. T. Lotze. 2007. Inside, outside, upside down: damage-associated molecular-pattern molecules (DAMPs) and redox. Trends Immunol. 28: 429-436.
76. Matzinger, P. 1994. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12: 991-1045.
77. Lotze, M. T., H. J. Zeh, A. Rubartelli, L. J. Sparvero, A. A. Amoscato, N. R. Washburn, M. E. Devera, X. Liang, M. Tör, and T. Billiar. 2007. The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol. Rev. 220: 60-81.
78. Hughes, R. C. 1999. Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim. Biophys. Acta 1473: 172-185.
79. Cherayil, B. J., S. J. Weiner, and S. Pillai. 1989. The Mac-2 antigen is a galactose-specific lectin that binds IgE. J. Exp. Med. 170: 1959-1972.
80. Sato, S. 2002. Galectins as molecules of danger signal, which could evoke an immune response to infection. Trends Glycoscience Glycotechnology 14: 285-301.
81. Sato, S., and J. Nieminen. 2004. Seeing strangers or announcing "danger": galectin-3 in two models of innate immunity. Glycoconj. J. 19: 583-591.
82. Sato, S., and G. A. Rabinovich. 2008. Galectins as danger signals in host-pathogen and host-tumor interactions: New members of the growing group of "alarmins"? In Galectins. A. A. Klysov, Z. J. Witczak, and D. Platt, eds. John Wiley & Sons, Inc., New York, p. 115-146.
83. Karlsson, A., P. Follin, H. Leffler, and C. Dahlgren. 1998. Galectin-3 activates the NADPH-oxidase in exudated but not peripheral blood neutrophils. Blood 91: 3430-3438.
84. Nieminen, J., C. St-Pierre, and S. Sato. 2005. Galectin-3 interacts with naive and primed neutrophils, inducing innate immune responses. J. Leukoc. Biol. 78: 1127-1135.
85. Kaye, P., and P. Scott. 2011. Leishmaniasis: complexity at the host-pathogen interface. Nat. Rev. Microbiol. 9: 604-615.
86. Pelletier, I., and S. Sato. 2002. Specific recognition and cleavage of galectin-3 by Leishmania major through species-specific polygalactose epitope. J. Biol. Chem. 277: 17663-17670.
87. Vasta, G. R. 2012. Galectins as pattern recognition receptors: structure, function, and evolution. Adv. Exp. Med. Biol. 946: 21-36.
88. Vasta, G. R. 2009. Roles of galectins in infection. Nat. Rev. Microbiol. 7: 424-438.
89. Kamhawi, S., M. Ramalho-Ortigao, V. M. Pham, S. Kumar, P. G. Lawyer, S. J. Turco, C. Barillas-Mury, D. L. Sacks, and J. G. Valenzuela. 2004. A role for insect galectins in parasite survival. Cell 119: 329-341.
90. Dobson, D. E., S. Kamhawi, P. Lawyer, S. J. Turco, S. M. Beverley, and D. L. Sacks. 2010. Leishmania major survival in selective Phlebotomus papatasi sand fly vector requires a specific SCG-encoded lipophosphoglycan galactosylation pattern. PLoS Pathog. 6: e1001185.
91. Zuberi, R. I., D. K. Hsu, O. Kalayci, H. Y. Chen, H. K. Sheldon, L. Yu, J. R. Apgar, T. Kawakami, C. M. Lilly, and F. T. Liu. 2004. Critical role for galectin-3 in airway inflammation and bronchial hyperresponsiveness in a murine model of asthma. Am. J. Pathol. 165: 2045-2053.
92. Bernardes, E. S., N. M. Silva, L. P. Ruas, J. R. Mineo, A. M. Loyola, D. K. Hsu, F. T. Liu, R. Chammas, and M. C. Roque-Barreira. 2006. Toxoplasma gondii infection reveals a novel regulatory role for galectin-3 in the interface of innate and adaptive immunity. Am. J. Pathol. 168: 1910-1920.
93. MacKinnon, A. C., S. L. Farnworth, P. S. Hodkinson, N. C. Henderson, K. M. Atkinson, H. Leffler, U. J. Nilsson, C. Haslett, S. J. Forbes, and T. Sethi. 2008. Regulation of alternative macrophage activation by galectin-3. J. Immunol. 180: 2650-2658.
94. Saegusa, J., D. K. Hsu, H. Y. Chen, L. Yu, A. Fermin, M. A. Fung, and F. T. Liu. 2009. Galectin-3 is critical for the development of the allergic inflammatory response in a mouse model of atopic dermatitis. Am. J. Pathol. 174: 922-931.
95. Demotte, N., V. Stroobant, P. J. Courtoy, P. Van Der Smissen, D. Colau, I. F. Luescher, C. Hivroz, J. Nicaise, J. L. Squifflet, M. Mourad, et al. 2008. Restoring the association of the T cell receptor with CD8 reverses anergy in human tumor-infiltrating lymphocytes. Immunity 28: 414-424.
96. Kropf, P., J. M. Fuentes, E. Fähnrich, L. Arpa, S. Herath, V. Weber, G. Soler, A. Celada, M. Modolell, and I. Müller. 2005. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. FASEB J. 19: 1000-1002.
97. Odegaard, J. I., R. R. Ricardo-Gonzalez, M. H. Goforth, C. R. Morel, V. Subramanian, L. Mukundan, A. Red Eagle, D. Vats, F. Brombacher, A. W. Ferrante, and A. Chawla. 2007.Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 447: 1116-1120.
98. St-Pierre, C., H. Manya, M. Ouellet, G. F. Clark, T. Endo, M. J. Tremblay, and S. Sato. 2011. Host-soluble galectin-1 promotes HIV-1 replication through a direct interaction with glycans of viral gp120 and host CD4. J. Virol. 85: 11742-11751.
99. Boscher, C., J. W. Dennis, and I. R. Nabi. 2011. Glycosylation, galectins and cellular signaling. Curr. Opin. Cell Biol. 23: 383-392.
100. Dennis, J. W., K. S. Lau, M. Demetriou, and I. R. Nabi. 2009. Adaptive regulation at the cell surface by N-glycosylation. Traffic 10: 1569-1578.
101. Lajoie, P., J. G. Goetz, J. W. Dennis, and I. R. Nabi. 2009. Lattices, rafts, and scaffolds: domain regulation of receptor signaling at the plasma membrane. J. Cell Biol. 185: 381-385.