Impacts of the apoptosis inhibitor of macrophage (AIM) on obesity-associated inflammatory diseases

Springer Science and Business Media LLC - Tập 36 - Trang 3-12 - 2013
Satoko Arai1, Toru Miyazaki1,2
1Laboratory of Molecular Biomedicine for Pathogenesis, Center for Disease Biology and Integrative Medicine, Faculty of Medicine, The University of Tokyo, Tokyo, Japan
2CREST, Japan Science and Technology Agency, Tokyo, Japan

Tóm tắt

Obesity is associated with various metabolic and cardiovascular diseases caused by chronic, low-grade inflammation that is initially observed in obese adipose tissue. In addition, many etiological studies in humans have shown a strong correlation between obesity and inflammatory autoimmune diseases. In this review, we focus on the involvement of apoptosis inhibitor of macrophage (AIM), a macrophage-derived blood protein, in both types of immune response. Through differential mechanisms, AIM thereby plays key roles in the pathogenesis of atherosclerosis, metabolic diseases, and obesity-associated autoimmune diseases. Thus, the regulation of blood AIM levels or AIM function has the potential to serve as a next-generation therapy against these inflammatory diseases brought about by modern lifestyle.

Tài liệu tham khảo

Hotamisligil GS, Shargill NS, Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259:87–91 Wellen KE, Hotamisligil GS (2003) Obesity-induced inflammatory changes in adipose tissue. J Clin Invest 112:1785–1788 Arkan MC, Hevener AL, Greten FR, Maeda S, Li ZW, Long JM, Wynshaw-Boris A, Poli G, Olefsky J, Karin M (2005) IKK-beta links inflammation to obesity-induced insulin resistance. Nat Med 11:191–198 Shoelson SE, Lee J, Goldfine AB (2006) Inflammation and insulin resistance. J Clin Invest 116:1793–1801 Neels JG, Olefsky JM (2006) Inflamed fat: what starts the fire? J Clin Invest 116:33–35 Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796–1808 Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112:1821–1830 Solinas G, Vilcu C, Neels JG, Bandyopadhyay GK, Luo JL, Naugler W, Grivennikov S, Wynshaw-Boris A, Scadeng M, Olefsky JM, Karin M (2007) JNK1 in hematopoietically derived cells contributes to diet-induced inflammation and insulin resistance without affecting obesity. Cell Metab 6:386–397 Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23–35 Gordon S, Taylor PR (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5:953–964 Lumeng CN, Bodzin JL, Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117:175–184 Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677–686 Rosenbloom AL (2003) Obesity, insulin resistance, beta-cell autoimmunity, and the changing clinical epidemiology of childhood diabetes. Diabetes Care 26:2954–2956 Hersoug LG, Linneberg A (2007) The link between the epidemics of obesity and allergic diseases: does obesity induce decreased immune tolerance? Allergy 62:1205–1213 Cambuli VM, Incani M, Cossu E, Congiu T, Scano F, Pilia S, Sentinelli F, Tiberti C, Cavallo MG, Loche S, Baroni MG (2010) Prevalence of type 1 diabetes autoantibodies (GADA, IA2, and IAA) in overweight and obese children. Diabetes Care 33:820–822 Marzullo P, Minocci A, Tagliaferri MA, Guzzaloni G, Di Blasio A, De Medici C, Aimaretti G, Liuzzi A (2010) Investigations of thyroid hormones and antibodies in obesity: leptin levels are associated with thyroid autoimmunity independent of bioanthropometric, hormonal, and weight-related determinants. J Clin Endocrinol Metab 95:3965–3972 Badaru A, Pihoker C (2012) Type 2 diabetes in childhood: clinical characteristics and role of β-cell autoimmunity. Curr Diab Rep 12:75–81 Winer DA, Winer S, Shen L, Wadia PP, Yantha J, Paltser G, Tsui H, Wu P, Davidson MG, Alonso MN, Leong HX, Glassford A, Caimol M, Kenkel JA, Tedder TF, McLaughlin T, Miklos DB, Dosch HM, Engleman EG (2011) B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 217:610–617 Miyazaki T, Hirokami Y, Matsuhashi N, Takatsuka H, Naito M (1999) Increased susceptibility of thymocytes to apoptosis in mice lacking AIM, a novel murine macrophage-derived soluble factor belonging to the scavenger receptor cysteine-rich domain superfamily. J Exp Med 189:413–422 Resnick D, Pearson A, Krieger M (1994) The SRCR superfamily: a family reminiscent of the Ig superfamily. Trends Biochem Sci 19:5–8 Mori M, Kimura H, Iwamura Y, Arai S, Miyazaki T (2012) Modification of N-glycosylation modulates the secretion and lipolytic function of apoptosis inhibitor of macrophage (AIM). FEBS Lett 586:3569–3574 Joseph SB, Bradley MN, Castrillo A, Bruhn KW, Mak PA, Pei L, Hogenesch J, O'Connell RM, Cheng G, Saez E, Miller JF, Tontonoz P (2004) LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell 119:299–309 Valledor AF, Hsu LC, Ogawa S, Sawka-Verhelle D, Karin M, Glass CK (2004) Activation of liver X receptors and retinoid X receptors prevents bacterial-induced macrophage apoptosis. Proc Natl Acad Sci U S A 101:17813–17818 Arai S, Shelton JM, Chen M, Bradley MN, Castrillo A, Bookout AL, Mak PA, Edwards PA, Mangelsdorf DJ, Tontonoz P, Miyazaki T (2005) A role of the apoptosis inhibitory factoAIM/Spα/Api6 in atherosclerosis development. Cell Metab 1:201–213 Miyazaki T, Kurokawa J, Arai S (2011) AIMing at metabolic syndrome. -Towards the development of novel therapies for metabolic diseases via apoptosis inhibitor of macrophage (AIM).-. Circ J 75:2522–2531 Gebe JA, Kiener PA, Ring HZ, Li X, Francke U, Aruffo A (1997) Molecular cloning, mapping to human chromosome 1 q21-q23, and cell binding characteristics of Spalpha, a new member of the scavenger receptor cysteine-rich (SRCR) family of proteins. J Biol Chem 272:6151–6158 Gebe JA, Llewellyn M, Hoggatt H, Aruffo A (2000) Molecular cloning, genomic organization and cell-binding characteristics of mouse Spalpha. Immunology 99:78–86 Gangadharan B, Antrobus R, Dwek RA, Zitzmann N (2007) Novel serum biomarker candidates for liver fibrosis in hepatitis C patients. Clin Chem 53:1792–1799 Kim WK, Hwang HR, do Kim H, Lee PY, In YJ, Ryu HY, Park SG, Bae KH, Lee SC (2009) Glycoproteomic analysis of plasma from patients with atopic dermatitis: CD5L and ApoE as potential biomarkers. Exp Mol Med 40:677–685 Gray J, Chattopadhyay D, Beale GS, Patman GL, Miele L, King BP, Stewart S, Hudson M, Day CP, Manas DM, Reeves HL (2009) A proteomic strategy to identify novel serum biomarkers for liver cirrhosis and hepatocellular cancer in individuals with fatty liver disease. BMC Cancer 9:271 Kurokawa J, Arai S, Nakashima K, Nagano H, Nishijima A, Miyata K, Ose R, Mori M, Kubota N, Kadowaki T, Oike Y, Koga H, Febbraio M, Iwanaga T, Miyazaki T (2010) AIM is endocytosed into adipocytes and decreases lipid droplets via inhibition of fatty acid synthase activity. Cell Metab 11:479–492 Arai S, Maehara N, Iwamura Y, Honda S, Nakashima K, Kai T, Ogishi M, Morita K, Kurokawa J, Mori M, Motoi Y, Miyake K, Matsuhashi N, Yamamura K, Ohara O, Shibuya A, Wakeland EK, Li QZ, Miyazaki T (2013) Obesity-associated autoantibody production requires AIM to retain IgM immune complex on follicular dendritic cells. Cell Rep 3:1187–1198 Yusa S, Ohnishi S, Onodera T, Miyazaki T (1999) AIM, a murine apoptosis inhibitory factor, induces strong and sustained growth inhibition of B lymphocytes in combination with TGF-β1. Eur J Immunol 29:1086–1093 Kuwata K, Watanabe H, Jiang SY, Yamamoto T, Tomiyama-Miyaji C, Abo T, Miyazaki T, Naito M (2003) AIM inhibits apoptosis of T cells and NKT cells in Corynebacterium-induced granuloma formation in mice. Am J Pathol 162:837–847 Qu P, Du H, Li Y, Yan C (2009) Myeloid-specific expression of Api6/AIM/Sp alpha induces systemic inflammation and adenocarcinoma in the lung. J Immunol 182:1648–1659 Vera J, Fenutría R, Cañadas O, Figueras M, Mota R, Sarrias MR, Williams DL, Casals C, Yelamos J, Lozano F (2009) The CD5 ectodomain interacts with conserved fungal cell wall components and protects from zymosan-induced septic shock-like syndrome. Proc Natl Acad Sci U S A 106:1506–1511 Akila P, Prashant V, Suma MN, Prashant SN, Chaitra TR (2012) CD163 and its expanding functional repertoire. Clin Chim Acta 413:669–674 Ligtenberg AJ, Veerman EC, Nieuw Amerongen AV, Mollenhauer J (2007) Salivary agglutinin/glycoprotein-340/DMBT1: a single molecule with variable composition and with different functions in infection, inflammation and cancer. Biol Chem 388:1275–1289 Martínez VG, Moestrup SK, Holmskov U, Mollenhauer J, Lozano F (2011) The conserved scavenger receptor cysteine-rich superfamily in therapy and diagnosis. Pharmacol Rev 63:967–1000 Zechner R, Strauss JG, Haemmerle G, Lass A, Zimmermann R (2005) Lipolysis: pathway under construction. Curr Opin Lipidol 16:333–340 Duncan RE, Ahmadian M, Jaworski K, Sarkadi-Nagy E, Sul HS (2007) Regulation of lipolysis in adipocytes. Annu Rev Nutr 27:79–101 Olsnes S, Klingenberg O, Wiedłocha A (2003) Transport of exogenous growth factors and cytokines to the cytosol and to the nucleus. Physiol Rev 83:163–182 Wesche J, Małecki J, Wiedłocha A, Skjerpen CS, Claus P, Olsnes S (2006) FGF-1 and FGF-2 require the cytosolic chaperone Hsp90 for translocation into the cytosol and the cell nucleus. J Biol Chem 281:11405–11412 Lin SY, Makino K, Xia W, Matin A, Wen Y, Kwong KY, Bourguignon L, Hung MC (2001) Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 3:802–808 Sandvig K, van Deurs B (2000) Entry of ricin and Shiga toxin into cells: molecular mechanisms and medical perspectives. EMBO J 19:5943–5950 Sandvig K, van Deurs B (2005) Delivery into cells: lessons learned from plant and bacterial toxins. Gene Ther 12:865–872 Ackerman AL, Kyritsis C, Tampé R, Cresswell P (2005) Access of soluble antigens to the endoplasmic reticulum can explain cross-presentation by dendritic cells. Nat Immunol 6:107–113 Giodini A, Cresswell P (2008) Hsp90-mediated cytosolic refolding of exogenous proteins internalized by dendritic cells. EMBO J 27:201–211 Wu Z, Rosen ED, Brun R, Hauser S, Adelmant G, Troy AE, McKeon C, Darlington GJ, Spiegelman BM (1999) Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Mol Cell 3:151–158 He W, Barak Y, Hevener A, Olson P, Liao D, Le J, Nelson M, Ong E, Olefsky JM, Evans RM (2003) Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc Natl Acad Sci U S A 100:15712–15717 Holm C (2003) Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans 31:1120–1124 Finn PF, Dice JF (2006) Proteolytic and lipolytic responses to starvation. Nutrition 22:830–844 Zechner R, Kienesberger PC, Haemmerle G, Zimmermann R, Lass A (2009) Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. J Lipid Res 50:3–21 Girousse A, Langin D (2012) Adipocyte lipases and lipid droplet-associated proteins: insight from transgenic mouse models. Int J Obes (Lond) 36:581–594 Lafontan M (2008) Advances in adipose tissue metabolism. Int J Obes 32(Suppl 7):S39–S51 Iwamura Y, Mori M, Nakashima K, Mikami T, Murayama K, Arai S, Miyazaki T (2012) Apoptosis inhibitor of macrophage (AIM) diminishes lipid droplet-coating proteins leading to lipolysis in adipocytes. Biochem Biophys Res Commun 422:476–481 Matsusue K (2010) A physiological role for fat specific protein 27/cell death-inducing DFF45-like effector C in adipose and liver. Biol Pharm Bull 33:346–350 Tontonoz P, Spiegelman BM (2008) Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 77:289–312 Tzameli I, Fang H, Ollero M, Shi H, Hamm JK, Kievit P, Hollenberg AN, Flier JS (2000) Regulated production of a peroxisome proliferator-activated receptor-gamma ligand during an early phase of adipocyte differentiation in 3T3-L1 adipocytes. J Biol Chem 279:36093–36102 Forman BM, Chen J, Evans RM (1997) Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc Natl Acad Sci U S A 94:4312–4317 Matsusue K, Kusakabe T, Noguchi T, Takiguchi S, Suzuki T, Yamano S, Gonzalez FJ (2008) Hepatic steatosis in leptin-deficient mice is promoted by the PPARgamma target gene Fsp27. Cell Metab 7:302–311 Dalen KT, Schoonjans K, Ulven SM, Weedon-Fekjaer MS, Bentzen TG, Koutnikova H, Auwerx J, Nebb HI (2007) Adipose tissue expression of the lipid droplet-associating proteins S3-12 and perilipin is controlled by peroxisome proliferator-activated receptor-gamma. Diabetes 53:1243–1252 Kurokawa J, Nagano H, Ohara O, Kubota N, Kadowaki T, Arai S, Miyazaki T (2011) Apoptosis inhibitor of macrophage (AIM) is required for obesity-associated recruitment of inflammatory macrophages into adipose tissue. Proc Natl Acad Sci U S A 108:12072–12077 Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116:3015–3025 Suganami T, Tanimoto-Koyama K, Nishida J, Itoh M, Yuan X, Mizuarai S, Kotani H, Yamaoka S, Miyake K, Aoe S, Kamei Y, Ogawa Y (2007) Role of the Toll-like receptor 4/NF-B pathway in saturated fatty acid-induced inflammatory changes in the interaction between adipocytes and macrophages. Arterioscler Thromb Vasc Biol 27:84–91 Poggi M, Bastelica D, Gual P, Iglesias MA, Gremeaux T, Knauf C, Peiretti F, Verdier M, Juhan-Vague I, Tanti JF, Burcelin R, Alessi MC (2007) C3H/HeJ mice carrying a toll-like receptor 4 mutation are protected against the development of insulin resistance in white adipose tissue in response to a high-fat diet. Diabetologia 50:1267–1276 Tsukumo DM, Carvalho-Filho MA, Carvalheira JB, Prada PO, Hirabara SM, Schenka AA, Araújo EP, Vassallo J, Curi R, Velloso LA, Saad MJ (2007) Loss-of-function mutation in Toll-like receptor 4 prevents diet-induced obesity and insulin resistance. Diabetes 56:1986–1998 Davis JE, Gabler NK, Walker-Daniels J, Spurlock ME (2008) Tlr-4 deficiency selectively protects against obesity induced by diets high in saturated fat. Obesity 16:1248–1255 Kamei N, Tobe K, Suzuki R, Ohsugi M, Watanabe T, Kubota N, Ohtsuka-Kowatari N, Kumagai K, Sakamoto K, Kobayashi M, Yamauchi T, Ueki K, Oishi Y, Nishimura S, Manabe I, Hashimoto H, Ohnishi Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Nagai R, Kadowaki T (2006) Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 281:26602–26614 Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R, Kitazawa S, Miyachi H, Maeda S, Egashira K, Kasuga M (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116:1494–1505 Keophiphath M, Rouault C, Divoux A, Clément K, Lacasa D (2010) CCL5 promotes macrophage recruitment and survival in human adipose tissue. Arterioscler Thromb Vasc Biol 30:39–45 Soma MR, Mims MP, Chari MV, Rees D, Morrisett JD (1992) Triglyceride metabolism in 3T3-L1 cells. An in vivo 13C NMR study. J Biol Chem 267:11168–11175 Kopp A, Gross P, Falk W, Bala M, Weigert J, Buechler C, Neumeier M, Schölmerich J, Schäffler A (2009) Fatty acids as metabolic mediators in innate immunity. Eur J Clin Invest 39:924–933 Schaeffler A, Gross P, Buettner R, Bollheimer C, Buechler C, Neumeier M, Kopp A, Schoelmerich J, Falk W (2009) Fatty acid-induced induction of Toll-like receptor-4/nuclear factor-kappaB pathway in adipocytes links nutritional signalling with innate immunity. Immunology 126:233–245 Miura T, Miki T (2009) GSK-3beta, a therapeutic target for cardiomyocyte protection. Circ J 73:1184–1192 Kantor AB, Herzenberg LA (1993) Origin of murine B cell lineages. Annu Rev Immunol 11:501–538 Hardy RR, Hayakawa K (1994) CD5 B cells, a fetal B cell lineage. Adv Immunol 55:297–339 Boes M (2000) Role of natural and immune IgM antibodies in immune responses. Mol Immunol 37:1141–1149 Pepys MB (1976) Role of complement in the induction of immunological responses. Transplant Rev 32:93–120 Ahearn JM, Fearon DT (1989) Structure and function of the complement receptors, CR1 (CD35) and CR2 (CD21). Adv Immunol 46:183–219 Heyman B (1990) The immune complex: possible ways of regulating the antibody response. Immunol Today 11:310–313 Carroll MC (1998) The role of complement and complement receptors in induction and regulation of immunity. Annu Rev Immunol 16:545–568 Allen CD, Cyster JG (2008) Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Semin Immunol 20:14–25 Tissot JD, Sanchez JC, Vuadens F, Scherl A, Schifferli JA, Hochstrasser DF, Schneider P, Duchosal MA (2002) IgM are associated to Sp alpha (CD5 antigen-like). Electrophoresis 23:1203–1206 Boes M, Esau C, Fischer MB, Schmidt T, Carroll M, Chen J (1998) Enhanced B-1 cell development, but impaired IgG antibody responses in mice deficient in secreted IgM. J Immunol 160:4776–4787 Shibuya A, Sakamoto N, Shimizu Y, Shibuya K, Osawa M, Hiroyama T, Eyre HJ, Sutherland GR, Endo Y, Fujita T, Miyabayashi T, Sakano S, Tsuji T, Nakayama E, Phillips JH, Lanier LL, Nakauchi H (2000) Fc alpha/mu receptor mediates endocytosis of IgM-coated microbes. Nat Immunol 1:441–446 Honda S, Kurita N, Miyamoto A, Cho Y, Usui K, Takeshita K, Takahashi S, Yasui T, Kikutani H, Kinoshita T, Fujita T, Tahara-Hanaoka S, Shibuya K, Shibuya A (2009) Enhanced humoral immune responses against T-independent antigens in Fc alpha/muR-deficient mice. Proc Natl Acad Sci U S A 106:11230–11235 MacLennan IC, Gray D, Kumararatne DS, Bazin H (1982) The lymphocytes of splenic marginal zones: a distinct B-cell lineage. Immunol Today 3:305–307 Lopes-Carvalho T, Kearney JF (2004) Development and selection of marginal zone B cells. Immunol Rev 197:192–205 Pillai S, Cariappa A, Moran ST (2005) Marginal zone B cells. Annu Rev Immunol 23:161–196 Oliver AM, Martin F, Kearney JF (1999) IgMhighCD21high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J Immunol 162:7198–7207 Meyer-Bahlburg A, Bandaranayake AD, Andrews SF, Rawlings DJ (2009) Reduced c-myc expression levels limit follicular mature B cell cycling in response to TLR signals. J Immunol 182:4065–4075 Li QZ, Xie C, Wu T, Mackay M, Aranow C, Putterman C, Mohan C (2005) Identification of autoantibody clusters that best predict lupus disease activity using glomerular proteome arrays. J Clin Invest 115:3428–3439 Li QZ, Zhou J, Wandstrat AE, Carr-Johnson F, Branch V, Karp DR, Mohan C, Wakeland EK, Olsen NJ (2007) Protein array autoantibody profiles for insights into systemic lupus erythematosus and incomplete lupus syndromes. Clin Exp Immunol 147:60–70 Li QZ, Zhou J, Lian Y, Zhang B, Branch VK, Carr-Johnson F, Karp DR, Mohan C, Wakeland EK, Olsen NJ (2010) Interferon signature gene expression is correlated with autoantibody profiles in patients with incomplete lupus syndromes. Clin Exp Immunol 159:281–291 Underhill GH, Minges Wols HA, Fornek JL, Witte PL, Kansas GS (2002) IgG plasma cells display a unique spectrum of leukocyte adhesion and homing molecules. Blood 99:2905–2912