Leptin as an immunological adjuvant: Enhanced migratory and CD8+ T cell stimulatory capacity of human dendritic cells exposed to leptin

FASEB Journal

Volumn 22, Issue 6, 2008, Pages 2012-2022

  Mattioli, Benedetta ^a   Straface, Elisabetta ^a   Matarrese, Paola ^a   Quaranta, Maria Giovanna ^a   Giordani, Luciana ^a   Malorni, Walter ^a   Viora, Marina ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Chemotaxis; CTL; Cytoskeleton; Vaccination

Indexed keywords

CD40 ANTIGEN; CHEMOKINE RECEPTOR CCR7; COFILIN; DENDRITIC CELL VACCINE; INTERLEUKIN 12P70; LEPTIN; LEPTIN RECEPTOR; RAC1 PROTEIN; VAV PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; CD8+ T LYMPHOCYTE; CELL MIGRATION; CELL SURVIVAL; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG EFFECT; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; MICROFILAMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TH1 CELL;

ADJUVANTS, IMMUNOLOGIC; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CYTOSKELETON; DENDRITIC CELLS; HUMANS; LEPTIN; LYMPHOCYTE ACTIVATION; SIGNAL TRANSDUCTION;

UROPODA;

EID: 44949172568     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-098095     Document Type: Article

References (75)

1. Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., and Friedman, J. M. (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 1, 425-432
2. Maffei, M., Fei, H., Lee, G. H., Dani, C., Leroy, P., Zhang, Y., Proenca, R., Negrel, R., Ailhaud, G., and Friedman, J. M. (1995) Increased expression in adipocytes of ob RNA in mice with lesions of the hypothalamus and with mutations at the db locus. Proc. Natl. Acad. Sci. U. S. A. 18, 6957-6960
3. Zhang, F., Basinski, M. B., Beals, J. M., Briggs, S. L., Churgay, L. M., Clawson, D. K., DiMarchi, R. D., Furman, T. C., Hale, J. E., Hsiung, H. M., Schoner, B. E., Smith, D. P., Zhang, X. Y., Wery, J. P., and Schevitz, R. W. (1997) Crystal structure of the obese protein leptin-E100. Nature 8, 206-209
4. Madej, T., Boguski, M. S., and Bryant, S. H. (1995) Threading analysis suggests that the obese gene product may be a helical cytokine. FEBS Lett. 2, 13-18
5. Flier, J. S. (1995) The adipocyte: storage depot or node on the energy information superhighway? Cell 13, 15-18
6. Considine, R. V., Sinha, M. K., Heiman, M. L., Kriauciunas, A., Stephens, T. W., Nyce, M. R., Ohannesian, J. P., Marco, C. C., McKee, L. J., and Bauer, T. L. (1996) Serum immunoreactiveleptin concentrations in normal-weight and obese humans. N. Engl. J. Med. 1, 292-295
7. Friedman, J. M. (1998) Leptin, leptin receptors, and the control of body weight. Nutr. Rev. 56(2 Pt. 2), s38-s46; discussion, s54-s75
8. Ahima, R.S., Prabakaran, D., Mantzoros, C., Qu, D., Lowell, B., Maratos-Flier, E., and Flier, J.S. (1996) Role of leptin in the neuroendocrine response to fasting. Nature 18, 250-252
9. Boden, G., Chen, X., Mozzoli, M., and Ryan, I. (1996) Effect of fasting on serum leptin in normal human subjects. J. Clin. Endocrinol. Metab. 81, 3419-3423
10. Grunfeld, C., Zhao, C., Fuller, J., Pollack, A., Moser, A., Friedman, J., and Feingold, K. R. (1996) Endotoxin and cytokines induce expression of leptin, the ob gene product, in hamsters. J. Clin. Invest. 97, 2152-2157
11. Janik, J. E., Curti, B. D., Considine, R. V., Rager, H. C., Powers, G. C., Alvord, W. G., Smith, J. W., Gause, B. L., and Kopp, W. C. (1997) Interleukin 1α increases serum leptin concentrations in humans. J. Clin. Endocrinol. Metab. 82, 3084-3086
12. White, D. W., and Tartaglia, L. A. (1996) Leptin and OB-R: body weight regulation by a cytokine receptor. Cytokine Growth Factor Rev. 7, 303-309
13. Tartaglia, L. A. (1997) The leptin receptor. J. Biol. Chem. 272, 6093-6096
14. Fei, H., Okano, H. J., Li, C., Lee, G. H., Zhao, C., Darnell, R., and Friedman, J. M. (1997) Anatomic localization of alternatively spliced leptin receptors (Ob-R) in mouse brain and other tissues. Proc. Natl. Acad. Sci. U. S. A. 94, 7001-7005
15. Cioffi, J. A., Shafer, A. W., and Zupancic, T. J. (1996) Novel B219/OB receptor isoforms: possible role of leptin in hematopoiesis and reproduction. Nat. Med. 2, 585-589
16. Gainsford, T., and Alexander, W. S. (1999) A role for leptin in hemopoiesis? Mol. Biotechnol. 11, 149-158
17. Lord, G. M., Matarese, G., Howard, J. K., Baker, R. J., Bloom, S. R., and Lechler, R. I. (1998) Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 394, 897-901
18. Zhao, Y., Sun, R., You, L., Gao, C., and Tian, Z. (2002) Expression of leptin receptors and response to leptin stimulation of human natural killer cell lines. Biochem. Biophys. Res. Commun. 300, 247-252
19. Sanchez-Margalet, V., Martin-Romero, C., Santos-Alvarez, J., Goberna, R., Najib, S., and Gonzalez-Yanes, C. (2003) Role of leptin as an immunomodulator of blood mononuclear cells: mechanisms of action. Clin. Exp. Immunol. 133, 11-19
20. Santos-Alvarez, J., Goberna, R., and Sanchez-Margalet, V. (1999) Human leptin stimulates proliferation and activation of human circulating monocytes. Cell. Immunol. 194, 6-11
21. Zarkesh-Esfahani, H., Pockley, A. G., Wu, Z., Hellewell, P. G., Weetman, A. P., and Ross, R. J. (2004) Leptin indirectly activates human neutrophils via induction of TNF-α. J. Immunol. 172, 1809-1814
22. Martin-Romero, C., Santos-Alvarez, J., Goberna, R., and Sanchez-Margalet, V. (2000) Human leptin enhances activation and proliferation of human circulating T lymphocytes. Cell. Immunol. 199, 15-24
23. La Cava, A., Alviggi, C., and Matarrese, G. (2004) Unravelling the multiple roles of leptin in inflammation and autoimmunity. J. Mol. Med. 82, 4-11
24. Mattioli, B., Straface, E., Quaranta, M. G., Giordani, L., and Viora, M. (2005) Leptin promotes differentiation and survival of human dendritic cells and licenses them for Th1 priming. J. Immunol. 174, 6820-6828
25. Lam, Q. L., Liu, S., Cao, X., and Lu, L. (2006) Involvement of leptin signaling in the survival and maturation of bone marrow-derived dendritic cells. Eur. J. Immunol. 36, 3118-3130
26. Macia, L., Delacre, M., Abboud, G., Ouk, T. S., Delanoye, A., Verwaerde, C., Saule, P., and Wolowczuk, I. (2006) Impairment of dendritic cell functionality and steady-state number in obese mice. J. Immunol. 77, 5997-6006
27. Steinman, R. M. (1999) Dendritic cells. In Fundamental Immunology, 4th Ed. (Paul, W. E., ed) pp. 547-573, Lippincott-Raven Publishers, Philadelphia
28. Banchereau, J., and Steinman, R. M. (1998) Dendritic cells and the control of immunity. Nature 392, 245-252
29. Sallusto, F., and Lanzavecchia, A. (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179, 1109-1118
30. Shutt, D. C., Daniels, K. J., Carolan, E. J., Hill, A. C., and Soll, D. R. (2000) Changes in the motility, morphology, and F-actin architecture of human dendritic cells in an in vitro model of dendritic cells development. Cell Motil. Cytoskeleton 46, 200-221
31. Granucci, F., Vizzardelli, C., Pavelka, N., Feau, S., Persico, M., Virzi, E., Rescigno, M., Moro, G., and Ricciardi-Castagnoli, P. (2001) Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat. Immunol. 2, 882-888
32. Sallusto, F., Palermo, B., Lenig, D., Miettinen, M., Matikainen, S., Julkunen, I., Forster, R., Burgstahler, R., Lipp, M., and Lanzavecchia, A. (1999) Distinct patterns and kinetics of chemokine production regulate dendritic cell function. Eur. J. Immunol. 29, 1617-1625
33. Ouaaz, F., Arron, J., Zheng, Y., Choi, Y., and Beg, A. A. (2002) Dendritic cell development and survival require distinct NF-B subunits. Immunity 16, 257-270
34. Jonuleit, H., Giesecke-Tuettenberg, A., Tuting, T., Thurner-Schuler, B., Stuge, T.B., Paragnik, L., Kandemir, A., Lee, P.P., Schuler, G., Knop, J., and Enk, A. H. A comparison of two types of dendritic cell as adjuvants for the induction of melanoma-specific T-cell responses in humans following intranodal injection. Int. J. Cancer 93, 243-251
35. Dhodapkar, M. V., Steinman, R. M., Krasovsky, J., Munz, C., and Bhardwaj, N. (2001) Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J. Exp. Med. 193, 233-238
36. De Vries, I. J., Lesterhuis, W. J., Scharenborg, N. M., Engelen, L. P., Ruiter, D. J., Gerritsen, M. J., Croockewit, S., Britten, C. M., Torensma, R., Adema, G. J., Figdor, C. G., and Punt, C. J. (2003) Maturation of dendritic cells is a prerequisite for inducing immune responses in advanced melanoma patients. Clin. Cancer Res. 9, 5091-5100
37. De Vries, I. J., Krooshoop, D. J., Scharenborg, N. M., Lesterhuis, W. J., Diepstra, J. H., Van Muijen, G. N., Strijk, S. P., Ruers, T. J., Boerman, O. C., Oyen, W. J., Adema, G. J., Punt, C. J., and Figdor, C. G. (2003) Effective migration of antigen-pulsed dendritic cells to lymph nodes in melanoma patients is determined by their maturation state. Cancer Res. 63, 12-17
38. Weber, A. (1999) Actin binding proteins that change extent and rate of actin monomer-polymer distribution by different mechanism. Mol. Cell. Biochem. 190, 67-74
39. Lane, P., Burdet, C., McConnell, F., Lanzavecchia, A., and Padovan, E. (1995) CD40 ligand-independent B cell activation revealed by CD40 ligand-deficient T cell clones: evidence for distinct activation requirements for antibody formation and B cell proliferation. Eur. J. Immunol. 25, 1788-1793
40. Malorni, W., Bari, M., Straface, E., Battista, N., Matarrese, P., Finazzi-Agro, A., Del Principe, D., and Maccarrone, M. (2004) Morphological evidence that 2-arachidonoylglycerol is a true agonist of human platelets. Thromb. Haemost. 92, 1159-1161
41. Quaranta, M. G., Mattioli, B., Spadaro, F., Straface, E., Giordani, L., Ramoni, C., Malorni, W., and Viora, M. (2003) HIV-1 Nef triggers Vav-mediated signaling pathway leading to functional and morphological differentiation of dendritic cells. FASEB J. 17, 2025-2036
42. Hanke, J. H., Gardner, J. P., and Dow, R. L. (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. J. Biol. Chem. 271, 695-701
43. Jaffe, A. B., and Hall, A. (2005) Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 1, 247-269
44. Benvenuti, F., Hugues, S., Walmsley, M., Ruf, S., Fetler, L., Popoff, M., Tybulewicz, V. L., and Amigorena, S. (2004) Requirement of Rac1 and Rac2 expression by mature dendritic cells for T cell priming. Science 305, 1150-1153
45. Langenkamp, A., Messi, M., Lanzavecchia, A., and Sallusto, F. (2000) Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat. Immunol. 1, 311-316
46. McIlroy, D., and Gregoire, M. (2003) Optimizing dendritic cell-based anticancer immunotherapy: maturation state does have clinical impact. Cancer Immunol. Immunother. 52, 583-591
47. Koch, F., Stanzl, U., Jennewein, P., Janke, K., Heufler, C., Kampgen, E., Romani, N., and Schuler, G. (1996) High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J. Exp. Med. 184, 741-746
48. Cella, M., Scheidegger, D., Palmer-Lehmann, K., Lane, P., Lanzavecchia, A., and Alber, G. (1996) Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184, 747-752
49. Lam, Q. L., Zheng, B. J., Jin, D. Y., Cao, X., and Lu, L. (2007) Leptin induces CD40 expression through the activation of Akt in murine dendritic cells. J. Biol. Chem. 282, 27587-27597
50. Banchereau, J., and Palucka, A. K. (2005) Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 5, 296-306
51. Turtle, C. J., and Hart, D. N. (2004) Dendritic cells in tumor immunology and immunotherapy. Curr. Drug Targets 5, 17-39
52. Granucci, F., Vizzardelli, C., Virzi, E., Rescigno, M., and Ricciardi-Castagnoli, P. (2001) Transcriptional reprogramming of dendritic cells by differentiation stimuli. Eur. J. Immunol. 31, 2539-2546
53. Randolph, G. J., Angeli, V., and Swartz, M. A. (2005) Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5, 617-628
54. Adema, G. J., de Vries, I. J., Punt, C. J., and Figdor, C. G. (2005) Migration of dendritic cell based cancer vaccines: in vivo veritas? Curr. Opin. Immunol. 17, 170-174
55. Rosenberg, S. A., Yang, J. C., and Restifo, N. P. (2004) Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 10, 909-915
56. Sallusto, F., Schaerli, P., Loetscher, P., Schaniel, C., Lenig, D., Mackay, C. R., Qin, S., and Lanzavecchia, A. (1998) Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur. J. Immunol. 28, 2760-2769
57. Hopken, U. E., Foss, H. D., Meyer, D., Hinz, M., Leder, K., Stein, H., and Lipp, M. (2002) Up-regulation of the chemokine receptor CCR7 in classical but not in lymphocyte-predominant Hodgkin disease correlates with distinct dissemination of neoplastic cells in lymphoid organs. Blood 99, 1109-1116
58. Sanchez-Sanchez, N., Riol-Blanco, L., and Rodriguez-Fernandez, J. L. (2006) The multiple personalities of the chemokine receptor CCR7 in dendritic cells. J. Immunol. 176, 5153-5159
59. Riol-Blanco, L., Sanchez-Sanchez, N., Torres, A., Tejedor, A., Narumiya, S., Corbi, A. L., Sanchez-Mateos, P., and Rodriguez-Fernandez, J. L. (2005) The chemokine receptor CCR7 activates in dendritic cells two signaling modules that independently regulate chemotaxis and migratory speed. J. Immunol. 174, 4070-4080
60. Chen, H., Bernstein, B. W., and Bamburg, J. R. (2000) Regulating actin-filament dynamics in vivo. Trends Biochem. Sci. 25, 19-23
61. Holt, M. R., and Koffer, A. (2001) Cell motility: proline-rich proteins promote protrusions. Trends Cell Biol. 11, 38-46
62. Verdijk, P., van Veelen, P. A., de Ru, A. H., Hensbergen, P. J., Mizuno, K., Koerten, H. K., Koning, F., Tensen, C. P., and Mommaas, A. M. (2004) Morphological changes during dendritic cell maturation correlate with cofilin activation and translocation to the cell membrane. Eur. J. Immunol. 34, 156-164
63. Gutzmer, R., Langer, K., Mommert, S., Wittmann, M., Kapp, A., and Werfel, T. (2003) Human dendritic cells express the IL-18R and are chemoattracted to IL-18. J. Immunol. 171, 6363-6371
64. O'Malley, D., Irving, A. J., and Harvey, J. (2005) Leptin-induced dynamic alterations in the actin cytoskeleton mediate the activation and synaptic clustering of BK channels. FASEB J. 19, 1917-1919
65. Saxena, N. K., Sharma, D., Ding, X., Lin, S., Marra, F., Merlin, D., and Anania, F. A. (2007) Concomitant activation of the JAK/STAT, PI3K/AKT, and ERK signaling is involved in leptin-mediated promotion of invasion and migration of hepatocellular carcinoma cells. Cancer Res. 67, 2497-2507
66. Attoub, S., Noe, V., Pirola, L., Bruyneel, E., Chastre, E., Mareel, M., Wymann, M. P., and Gespach, C. (2000) Leptin promotes invasiveness of kidney and colonic epithelial cells via phosphoinositide 3-kinase-, Rho-, and Rac-dependent signaling pathways. FASEB J. 14, 2329-2338
67. Ridley, A. J. (2001) Rho GTPases and cell migration. J. Cell Sci. 114, 2713-2722
68. Giammarioli, A. M., Gambardella, L., Quaranta, M. G., Lapenta, C., Santini, S. M., Belardelli, F., Viora, M., and Malorni, W. (2006) Differentiation of monocyte-derived dendritic cells is associated with upregulation and activation of Rac-1 small GTPase. FEBS Lett. 580, 3335-3339
69. Jaffe, A. B., and Hall, A. (2005) Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269
70. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T., and Horwitz, A. R. (2003) Cell migration: integrating signals from front to back. Science 302, 1704-1709
71. Fruhbeck, G. (2006) Intracellular signalling pathways activated by leptin. Biochem. J. 393, 7-20
72. Luft, T., Maraskovsky, E., Schnurr, M., Knebel, K., Kirsch, M., Gorner, M., Skoda, R., Ho, A. D., Nawroth, P., and Bierhaus, A. (2004) Tuning the volume of the immune response: strength and persistence of stimulation determine migration and cytokine secretion of dendritic cells. Blood 104, 1066-1074
73. Berard, F., Blanco, P., Davoust, J., Neidhart-Berard, E. M., Nouri-Shirazi, M., Taquet, N., Rimoldi, D., Cerottini, J. C., Banchereau, J., and Palucka, A. K. (2000) Cross-priming of naive CD8 T cells against melanoma antigens using dendritic cells loaded with killed allogeneic melanoma cells. J. Exp. Med. 192, 1535-1544
74. Shankaran, V., Ikeda, H., Bruce, A. T., White, J. M., Swanson, P. E., Old, L. J., and Schreiber, R. D. (2001) IFNγ and lymphocytes prevent primary tumor development and shape tumor immunogenicity. Nature 410, 1107-1111
75. Gao, Y., Tao, J., M.O, Li., Zhang, D., Chi, H., Henegariu, O., Kaech, S. M., Davis, R. J., Flavell, R. A., and Yin, Z. (2005) JNK1 is essential for CD8+ T cell-mediated tumor immune surveillance. J. Immunol. 175, 5783-5789