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

Seminars in Immunopathology

Volumn 36, Issue 1, 2014, Pages 3-12

  Arai, Satoko ^a   Miyazaki, Toru ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

AIM (apoptosis inhibitor of macrophage); Autoantibody; Chronic inflammation; IgM; Lipolysis

Indexed keywords

APOPTOSIS INHIBITOR OF MACROPHAGE; AUTOANTIBODY; FAT DROPLET; FC RECEPTOR; FCALPHA RECEPTOR; FCMU RECEPTOR; IMMUNOGLOBULIN M; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PLASMA PROTEIN; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOSE TISSUE; ANTIBODY PRODUCTION; ATHEROSCLEROSIS; AUTOIMMUNITY; B LYMPHOCYTE; BINDING KINETICS; CELL MIGRATION; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; FAT MASS; HUMAN; INFLAMMATORY DISEASE; INSULIN RESISTANCE; LIPOLYSIS; MACROPHAGE; METABOLIC DISORDER; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SPLEEN;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; AUTOANTIBODIES; AUTOIMMUNITY; B-LYMPHOCYTES; DISEASE SUSCEPTIBILITY; HUMANS; IMMUNOGLOBULIN M; INFLAMMATION; INHIBITOR OF APOPTOSIS PROTEINS; INSULIN RESISTANCE; LIPOLYSIS; MACROPHAGES; METABOLIC SYNDROME X; MICE; MICE, KNOCKOUT; OBESITY; PPAR GAMMA; RECEPTORS, FC; SPLEEN; TOLL-LIKE RECEPTOR 4;

EID: 84895888255     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-013-0405-5     Document Type: Review

References (96)

1. 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 (Pubitemid 23036092)
2. Wellen KE, Hotamisligil GS (2003) Obesity-induced inflammatory changes in adipose tissue. J Clin Invest 112:1785-1788 (Pubitemid 38063699)
3. 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 (Pubitemid 40321355)
4. Shoelson SE, Lee J, Goldfine AB (2006) Inflammation and insulin resistance. J Clin Invest 116:1793-1801 (Pubitemid 44033299)
5. Neels JG, Olefsky JM(2006) Inflamed fat: what starts the fire? J Clin Invest 116:33-35 (Pubitemid 43121788)
6. 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 (Pubitemid 38063703)
7. 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 (Pubitemid 38063705)
8. 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 (Pubitemid 350012000)
9. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3:23-35
10. Gordon S, Taylor PR (2005)Monocyte and macrophage heterogeneity. Nat Rev Immunol 5:953-964 (Pubitemid 41746764)
11. Lumeng CN, Bodzin JL, Saltiel AR (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117:175-184 (Pubitemid 46048464)
12. 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 (Pubitemid 39457982)
13. Rosenbloom AL (2003) Obesity, insulin resistance, beta-cell autoimmunity, and the changing clinical epidemiology of childhood diabetes. Diabetes Care 26:2954-2956
14. 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
15. 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
16. 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
17. Badaru A, Pihoker C (2012) Type 2 diabetes in childhood: clinical characteristics and role of β-cell autoimmunity. Curr Diab Rep 12:75-81
18. 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
19. 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 (Pubitemid 29063262)
20. Resnick D, Pearson A, Krieger M (1994) The SRCR superfamily: a family reminiscent of the Ig superfamily. Trends Biochem Sci 19:5-8 (Pubitemid 24028723)
21. 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
22. 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 (Pubitemid 39360910)
23. 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 (Pubitemid 40051969)
24. 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 (Pubitemid 43960602)
25. 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
26. 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 (Pubitemid 27118082)
27. Gebe JA, Llewellyn M, Hoggatt H, Aruffo A (2000) Molecular cloning, genomic organization and cell-binding characteristics of mouse Spalpha. Immunology 99:78-86 (Pubitemid 30062941)
28. 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 (Pubitemid 47509672)
29. 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
30. 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
31. 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) AIMis endocytosed into adipocytes and decreases lipid droplets via inhibition of fatty acid synthase activity. Cell Metab 11:479-492
32. 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
33. 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 (Pubitemid 29164153)
34. 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 (Pubitemid 36237492)
35. 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
36. 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
37. Akila P, Prashant V, Suma MN, Prashant SN, Chaitra TR (2012) CD163 and its expanding functional repertoire. Clin Chim Acta 413:669-674
38. 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 (Pubitemid 350135572)
39. 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
40. Zechner R, Strauss JG, Haemmerle G, Lass A, Zimmermann R (2005) Lipolysis: pathway under construction. Curr Opin Lipidol 16:333-340 (Pubitemid 40839763)
41. Duncan RE, Ahmadian M, Jaworski K, Sarkadi-Nagy E, Sul HS (2007) Regulation of lipolysis in adipocytes. Annu Rev Nutr 27:79-101 (Pubitemid 351373349)
42. 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 (Pubitemid 36459880)
43. 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 (Pubitemid 43855565)
44. 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 (Pubitemid 32842685)
45. Sandvig K, van Deurs B (2000) Entry of ricin and Shiga toxin into cells: molecular mechanisms and medical perspectives. EMBO J 19:5943-5950
46. Sandvig K, van Deurs B (2005) Delivery into cells: lessons learned from plant and bacterial toxins. Gene Ther 12:865-872 (Pubitemid 40852204)
47. 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 (Pubitemid 40136702)
48. Giodini A, Cresswell P (2008) Hsp90-mediated cytosolic refolding of exogenous proteins internalized by dendritic cells. EMBO J 27:201-211
49. 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 (Pubitemid 29292616)
50. 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 (Pubitemid 38021055)
51. Holm C (2003) Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans 31:1120-1124
52. Finn PF, Dice JF (2006) Proteolytic and lipolytic responses to starvation. Nutrition 22:830-844 (Pubitemid 43947502)
53. 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
54. Girousse A, Langin D (2012) Adipocyte lipases and lipid droplet-associated proteins: insight from transgenic mouse models. Int J Obes (Lond) 36:581-594
55. Lafontan M (2008) Advances in adipose tissue metabolism. Int J Obes 32(Suppl 7):S39-S51
56. 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
57. 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
58. Tontonoz P, Spiegelman BM (2008) Fat and beyond: the diverse biology of PPARgamma. Annu Rev Biochem 77:289-312
59. 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 (Pubitemid 39100617)
60. 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 (Pubitemid 27194238)
61. 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 (Pubitemid 351455219)
62. 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 (Pubitemid 38569010)
63. 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
64. 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 (Pubitemid 44684486)
65. 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 (Pubitemid 46370478)
66. 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 (Pubitemid 46701560)
67. 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 (Pubitemid 47195825)
68. 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 (Pubitemid 351770507)
69. 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 (Pubitemid 44401869)
70. 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
71. 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
72. 13CNMR study. J Biol Chem 267:11168-11175
73. 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
74. 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
75. Miura T, Miki T (2009) GSK-3beta, a therapeutic target for cardiomyocyte protection. Circ J 73:1184-1192
76. Kantor AB, Herzenberg LA (1993) Origin of murine B cell lineages. Annu Rev Immunol 11:501-538 (Pubitemid 23115016)
77. Hardy RR, Hayakawa K (1994) CD5 B cells, a fetal B cell lineage. Adv Immunol 55:297-339 (Pubitemid 24057056)
78. Boes M (2000) Role of natural and immune IgM antibodies in immune responses. Mol Immunol 37:1141-1149
79. Pepys MB (1976) Role of complement in the induction of immunological responses. Transplant Rev 32:93-120
80. Ahearn JM, Fearon DT (1989) Structure and function of the complement receptors, CR1 (CD35) and CR2 (CD21). Adv Immunol 46:183-219 (Pubitemid 19254752)
81. Heyman B (1990) The immune complex: possible ways of regulating the antibody response. Immunol Today 11:310-313
82. Carroll MC (1998) The role of complement and complement receptors in induction and regulation of immunity. Annu Rev Immunol 16:545-568
83. Allen CD, Cyster JG (2008) Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Semin Immunol 20:14-25
84. 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
85. 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 (Pubitemid 28215311)
86. 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
87. 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
88. 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
89. Lopes-Carvalho T, Kearney JF (2004) Development and selection of marginal zone B cells. Immunol Rev 197:192-205 (Pubitemid 38142177)
90. Pillai S, Cariappa A, Moran ST (2005) Marginal zone B cells. Annu Rev Immunol 23:161-196 (Pubitemid 40563168)
91. 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 (Pubitemid 29277691)
92. Meyer-Bahlburg A, Bandaranayake AD, Andrews SF, Rawlings DJ (2009) Reduced c-myc expression levels limit follicularmature B cell cycling in response to TLR signals. J Immunol 182:4065-4075
93. 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 (Pubitemid 43121831)
94. 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 (Pubitemid 44915556)
95. 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
96. 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 (Pubitemid 34525380)