Short-term and long-term leptin exposure differentially affect human natural killer cell immune functions

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 1, 2012, Pages

  Wrann, Christiane D ^a,b   Laue, Tobias ^b   Hübner, Lena ^b   Kuhlmann, Susanne ^b   Jacobs, Roland ^b   Goudeva, Lilia ^b   Nave, Heike ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Adipokine; Immunity; Obesity

Indexed keywords

CD16 ANTIGEN; GAMMA INTERFERON; JANUS KINASE 2; LEPTIN; LEPTIN RECEPTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL CELL; ARTICLE; CANCER SUSCEPTIBILITY; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; NATURAL KILLER CELL; NONHUMAN; OBESITY; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; CYTOPHAGOCYTOSIS; GENE EXPRESSION REGULATION; HUMANS; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LEPTIN; MICE; NEOPLASMS; OBESITY; PROTEIN ISOFORMS; RECEPTORS, IGG; RECEPTORS, LEPTIN; RECOMBINANT PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 83455198332     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00057.2011     Document Type: Article

References (61)

1. Ahima RS, Flier JS. Leptin. Annu Rev Physiol 62: 413-437, 2000.
2. Akesson C, Uvebrant K, Oderup C, Lynch K, Harris RA, Lernmark A, Agardh CD, Cilio CM. Altered natural killer (NK) cell frequency and phenotype in latent autoimmune diabetes in adults (LADA) prior to insulin deficiency. Clin Exp Immunol 161: 48-56, 2010.
3. Aleffi S, Petrai I, Bertolani C, Parola M, Colombatto S, Novo E, Vizzutti F, Anania FA, Milani S, Rombouts K, Laffi G, Pinzani M, Marra F. Upregulation of proinflammatory and proangiogenic cytokines by leptin in human hepatic stellate cells. Hepatology 42: 1339-1348, 2005.
4. Badman MK, Flier JS. The adipocyte as an active participant in energy balance and metabolism. Gastroenterology 132: 2103-2115, 2007.
5. Baumann H, Morella KK, White DW, Dembski M, Bailon PS, Kim H, Lai CF, Tartaglia LA. The full-length leptin receptor has signaling capabilities of interleukin 6-type cytokine receptors. Proc Natl Acad Sci USA 93: 8374-8378, 1996.
6. Bjørbaek C, Elmquist JK, Frantz JD, Shoelson SE, Flier JS. Identification of SOCS-3 as a potential mediator of central leptin resistance. Mol Cell 1: 619-625, 1998.
7. Bjorbaek C, Uotani S, da Silva B, Flier JS. Divergent signaling capacities of the long and short isoforms of the leptin receptor. J Biol Chem 272: 32686-32695, 1997.
8. Brauner H, Elemans M, Lemos S, Broberger C, Holmberg D, Flodström-Tullberg M, Kärre K, Höglund P. Distinct phenotype and function of NK cells in the pancreas of nonobese diabetic mice. J Immunol 184: 2272-2280, 2010.
9. Bryant J, Day R, Whiteside TL, Herberman RB. Calculation of lytic units for the expression of cell-mediated cytotoxicity. J Immunol Methods 146: 91-103, 1992.
10. Caldefie-Chezet F, Poulin A, Vasson MP. Leptin regulates functional capacities of polymorphonuclear neutrophils. Free Radic Res 37: 809-814, 2003.
11. Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 4: 579-591, 2004.
12. Caspar-Bauguil S, Cousin B, Andre M, Nibbelink M, Galinier A, Periquet B, Casteilla L, Penicaud L. Weight-dependent changes of immune system in adipose tissue: importance of leptin. Exp Cell Res 312: 2195-2202, 2006.
13. Caspar-Bauguil S, Cousin B, Galinier A, Segafredo C, Nibbelink M, Andre M, Casteilla L, Penicaud L. Adipose tissues as an ancestral immune organ: site-specific change in obesity. FEBS Lett 579: 3487-3492, 2005.
14. Chandra RK. Cell-mediated immunity in genetically obese C57BL/6J (ob/ob) mice. Am J Clin Nutr 33: 13-16, 1980.
15. Cottam DR, Schaefer PA, Shaftan GW, Angus LD. Dysfunctional immune-privilege in morbid obesity: implications and effect of gastric bypass surgery. Obes Surg 13: 49-57, 2003.
16. Dovio A, Caramello V, Masera RG, Sartori ML, Saba L, Tinivella M, Prolo P, Termine A, Avagnina P, Angeli A. Natural killer cell activity and sensitivity to positive and negative modulation in uncomplicated obese subjects: relationships to leptin and diet composition. Int J Obes Relat Metab Disord 28: 894-901, 2004.
17. Elinav E, Abd-Elnabi A, Pappo O, Bernstein I, Klein A, Engelhardt D, Rabbani E, Ilan Y. Suppression of hepatocellular carcinoma growth in mice via leptin, is associated with inhibition of tumor cell growth and natural killer cell activation. J Hepatol 44: 529-536, 2006.
18. Farooqi IS, Matarese G, Lord GM, Keogh JM, Lawrence E, Agwu C, Sanna V, Jebb SA, Perna F, Fontana S, Lechler RI, DePaoli AM, O'Rahilly S. Beneficial effects of leptin on obesity, T cell hyporesponsiveness, and neuroendocrine/metabolic dysfunction of human congenital leptin deficiency. J Clin Invest 110: 1093-1103, 2002.
19. Fernández-Riejos P, Najib S, Santos-Alvarez J, Martín-Romero C, Pérez-Pérez A, González-Yanes C, Sánchez-Margalet V. Role of leptin in the activation of immune cells. Mediators Inflamm 2010: 568343, 2010.
20. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, Lee J, Goldfine AB, Benoist C, Shoelson S, Mathis D. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 15: 930-939, 2009.
21. Flegal KM, Graubard BI, Williamson DF, Gail MH. Sources of differences in estimates of obesity-associated deaths from first National Health and Nutrition Examination Survey (NHANES I) hazard ratios. Am J Clin Nutr 91: 519-527, 2010.
22. Ghilardi N, Ziegler S, Wiestner A, Stoffel R, Heim MH, Skoda RC. Defective STAT signaling by the leptin receptor in diabetic mice. Proc Natl Acad Sci USA 93: 6231-6235, 1996.
23. Gibson WT, Farooqi IS, Moreau M, DePaoli AM, Lawrence E, O'Rahilly S, Trussell RA. Congenital leptin deficiency due to homozygosity for the Delta133G mutation: report of another case and evaluation of response to four years of leptin therapy. J Clin Endocrinol Metab 89: 4821-4826, 2004.
24. Jacobs R, Hintzen G, Kemper A, Beul K, Kempf S, Behrens G, Sykora KW, Schmidt RE. CD56bright cells differ in their KIR repertoire and cytotoxic features from CD56dim NK cells. Eur J Immunol 31: 3121-3127, 2001.
25. Jacobs R, Pawlak CR, Mikeska E, Meyer-Olson D, Martin M, Heijnen CJ, Schedlowski M, Schmidt RE. Systemic lupus erythematosus and rheumatoid arthritis patients differ from healthy controls in their cytokine pattern after stress exposure. Rheumatology (Oxford) 40: 868-875, 2001.
26. Kanda T, Takahashi T, Kudo S, Takeda T, Tsugawa H, Takekoshi N. Leptin deficiency enhances myocardial necrosis and lethality in a murine model of viral myocarditis. Life Sci 75: 1435-1447, 2004.
27. Key TJ, Appleby PN, Reeves GK, Roddam A, Dorgan JF, Longcope C, Stanczyk FZ, Stephenson HE Jr, Falk RT, Miller R, Schatzkin A, Allen DS, Fentiman IS, Key TJ, Wang DY, Dowsett M, Thomas HV, Hankinson SE, Toniolo P, Akhmedkhanov A, Koenig K, Shore RE, Zeleniuch-Jacquotte A, Berrino F, Muti P, Micheli A, Krogh V, Sieri S, Pala V, Venturelli E, Secreto G, Barrett-Connor E, Laughlin GA, Kabuto M, Akiba S, Stevens RG, Neriishi K, Land CE, Cauley JA, Kuller LH, Cummings SR, Helzlsouer KJ, Alberg AJ, Bush TL, Comstock GW, Gordon GB, Miller SR, Longcope C; Endogenous Hormones Breast Cancer Collaborative Group. Body mass index, serum sex hormones, and breast cancer risk in postmenopausal women. J Natl Cancer Inst 95: 1218-1226, 2003.
28. Key TJ, Appleby PN, Reeves GK, Roddam AW. Insulin-like growth factor 1 (IGF1), IGF binding protein 3 (IGFBP3), and breast cancer risk: pooled individual data analysis of 17 prospective studies. Lancet Oncol 11: 530-542, 2010.
29. La Cava A, Matarese G. The weight of leptin in immunity. Nat Rev Immunol 4: 371-379, 2004.
30. Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 9: 495-502, 2008.
31. Lautenbach A, Wrann CD, Jacobs R, Muller G, Brabant G, Nave H. Altered phenotype of NK cells from obese rats can be normalized by transfer into lean animals. Obesity (Silver Spring) 17: 1848-1855, 2009.
32. Lo CK, Lam QL, Yang M, Ko KH, Sun L, Ma R, Wang S, Xu H, Tam S, Wu CY, Zheng BJ, Lu L. Leptin signaling protects NK cells from apoptosis during development in mouse bone marrow. Cell Mol Immunol 6: 353-360, 2009.
33. Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI. Leptin modulates the T-cell immune response and reverses starvationinduced immunosuppression. Nature 394: 897-901, 1998.
34. Lynch LA, O'Connell JM, Kwasnik AK, Cawood TJ, O'Farrelly C, O'Shea DB. Are natural killer cells protecting the metabolically healthy obese patient? Obesity (Silver Spring) 17: 601-605, 2009.
35. MacDougald OA, Hwang CS, Fan H, Lane MD. Regulated expression of the obese gene product (leptin) in white adipose tissue and 3T3-L1 adipocytes. Proc Natl Acad Sci USA 92: 9034-9037, 1995.
36. Martín-Romero C, Santos-Alvarez J, Goberna R, Sánchez-Margalet V. Human leptin enhances activation and proliferation of human circulating T lymphocytes. Cell Immunol 199: 15-24, 2000.
37. Mori A, Sakurai H, Choo MK, Obi R, Koizumi K, Yoshida C, Shimada Y, Saiki I. Severe pulmonary metastasis in obese and diabetic mice. Int J Cancer 119: 2760-2767, 2006.
38. Moriguchi S, Oonishi K, Kato M, Kishino Y. Obesity is a risk factor for deteriorating cellular immune functions decreased with aging. Nutr Res 15: 151-160, 1995.
39. Moulin CM, Marguti I, Peron JP, Halpern A, Rizzo LV. Bariatric surgery reverses natural killer (NK) cell activity and NK-related cytokine synthesis impairment induced by morbid obesity. Obes Surg 21: 112-118, 2011.
40. Nave H, Mueller G, Siegmund B, Jacobs R, Stroh T, Schueler U, Hopfe M, Behrendt P, Buchenauer T, Pabst R, Brabant G. Resistance of Janus kinase-2 dependent leptin signaling in natural killer (NK) cells: a novel mechanism of NK cell dysfunction in diet-induced obesity. Endocrinology 149: 3370-3378, 2008.
41. Nguyen DM, El-Serag HB. The epidemiology of obesity. Gastroenterol Clin North Am 39: 1-7, 2010.
42. O'Rourke RW, Metcalf MD, White AE, Madala A, Winters BR, Maizlin II, Jobe BA, Roberts CT Jr, Slifka MK, Marks DL. Depotspecific differences in inflammatory mediators and a role for NK cells and IFN-gamma in inflammation in human adipose tissue. Int J Obes (Lond) 33: 978-990, 2009.
43. O'Shea D, Cawood TJ, O'Farrelly C, Lynch L. Natural killer cells in obesity: impaired function and increased susceptibility to the effects of cigarette smoke. PLoS One 5: e8660, 2010.
44. Otero M, Lago R, Gomez R, Dieguez C, Lago F, Gómez-Reino J, Gualillo O. Towards a pro-inflammatory and immunomodulatory emerging role of leptin. Rheumatology (Oxford) 45: 944-950, 2006.
45. Pisani P. Hyper-insulinaemia and cancer, meta-analyses of epidemiological studies. Arch Physiol Biochem 114: 63-70, 2008.
46. Renehan AG, Roberts DL, Dive C. Obesity and cancer: pathophysiological and biological mechanisms. Arch Physiol Biochem 114: 71-83, 2008.
47. Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet 371: 569-578, 2008.
48. Rosen ED, Spiegelman BM. Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444: 847-853, 2006.
49. Smith AG, Sheridan PA, Harp JB, Beck MA. Diet-induced obese mice have increased mortality and altered immune responses when infected with influenza virus. J Nutr 137: 1236-1243, 2007.
50. Sun Y, Lodish HF. Adiponectin deficiency promotes tumor growth in mice by reducing macrophage infiltration. PLoS One 5: e11987, 2010.
51. Takahashi T, Yu F, Saegusa S, Sumino H, Nakahashi T, Iwai K, Morimoto S, Kurabayashi M, Kanda T. Impaired expression of cardiac adiponectin in leptin-deficient mice with viral myocarditis. Int Heart J 47: 107-123, 2006.
52. Tian Z, Sun R, Wei H, Gao B. Impaired natural killer (NK) cell activity in leptin receptor deficient mice: leptin as a critical regulator in NK cell development and activation. Biochem Biophys Res Commun 298: 297-302, 2002.
53. Tilg H, Hotamisligil GS. Nonalcoholic fatty liver disease: Cytokineadipokine interplay and regulation of insulin resistance. Gastroenterology 131: 934-945, 2006.
54. Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol 6: 772-783, 2006.
55. Villanueva EC, Myers MG Jr. Leptin receptor signaling and the regulation of mammalian physiology. Int J Obes (Lond) 32, Suppl 7: S8-S12, 2008.
56. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol 9: 503-510, 2008.
57. Vona-Davis L, Rose DP. Adipokines as endocrine, paracrine, and autocrine factors in breast cancer risk and progression. Endocr Relat Cancer 14: 189-206, 2007.
58. Wolpin BM, Michaud DS, Giovannucci EL, Schernhammer ES, Stampfer MJ, Manson JE, Cochrane BB, Rohan TE, Ma J, Pollak MN, Fuchs CS. Circulating insulin-like growth factor binding protein-1 and the risk of pancreatic cancer. Cancer Res 67: 7923-7928, 2007.
59. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature 372: 425-432, 1994.
60. Zhao T, Hou M, Xia M, Wang Q, Zhu H, Xiao Y, Tang Z, Ma J, Ling W. Globular adiponectin decreases leptin-induced tumor necrosis factoralpha expression by murine macrophages: involvement of cAMP-PKA and MAPK pathways. Cell Immunol 238: 19-30, 2005.
61. Zhao Y, Sun R, You L, Gao C, Tian Z. Expression of leptin receptors and response to leptin stimulation of human natural killer cell lines. Biochem Biophys Res Commun 300: 247-252, 2003