AIM associated with the IgM pentamer: attackers on stand-by at aircraft carrier

Cellular and Molecular Immunology

Volumn 15, Issue 6, 2018, Pages 563-574

  Miyazaki, Toru ^a,b,c   Yamazaki, Tomoko ^a   Sugisawa, Ryoichi ^a   Gershwin, M Eric ^d   Arai, Satoko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN AGENCY FOR MEDICAL RESEARCH AND DEVELOPMENT   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS INHIBITOR OF MACROPHAGE PROTEIN; CELL PROTEIN; FAT; FC ALPHA RECEPTOR; FC MICRO RECEPTOR; FC RECEPTOR; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M; UNCLASSIFIED DRUG; AUTOANTIBODY; POLYMERIC IGM; SCAVENGER RECEPTOR;

ACUTE KIDNEY FAILURE; ANTIBODY PRODUCTION; ANTIGEN BINDING; ANTIGEN PRESENTATION; B LYMPHOCYTE; BACTERIUM; CANCER CELL; CELL STIMULATION; DENDRITIC CELL; DISEASE ASSOCIATION; DISEASE EXACERBATION; DISEASE PREDISPOSITION; GERMINAL CENTER; GLOMERULUS; HUMAN; INTERNALIZATION; KIDNEY PROXIMAL TUBULE; NONHUMAN; OBESITY; OVARY FOLLICLE CELL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SECRETION; REVIEW; SPLEEN CELL; URINARY EXCRETION; ANIMAL; BLOOD; CHEMISTRY; IMMUNOLOGY; METABOLISM; PATHOLOGY; URINE;

ACUTE KIDNEY INJURY; ANIMALS; AUTOANTIBODIES; DISEASE PROGRESSION; HUMANS; IMMUNOGLOBULIN M; RECEPTORS, SCAVENGER;

EID: 85051242274     PISSN: 16727681     EISSN: None     Source Type: Journal    
DOI: 10.1038/cmi.2017.141     Document Type: Review

References (80)

1. Miyazaki T, Hirokami Y, Matsuhashi N, Takatsuka H, Naito M. 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 1999; 189: 413–422
2. Arai S, Maehara N, Iwamura Y, Honda S, Nakashima K, Kai T et al. Obesity-associated autoantibody production requires AIM to retain IgM immune complex on follicular dendritic cells. Cell Rep 2013; 3: 1187–1198
3. Yamazaki T, Mori M, Arai S, Tateishi R, Abe M, Ban M et al. Circulating AIM as an indicator of liver damage and hepatocellular carcinoma in humans. PLoS One 2014; 9: e109123
4. Resnick D, Pearson A, Krieger M. The SRCR superfamily: a family reminiscent of the Ig superfamily. Trends Biochem Sci 1994; 19: 5–8
5. Gebe JA, Kiener PA, Ring HZ, Li X, Francke U, Aruffo A. 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 1997; 272: 6151–6158
6. Mori M, Kimura H, Iwamura Y, Arai S, Miyazaki T. Modification of N-glycosylation modulates the secretion and lipolytic function of apoptosis inhibitor of macrophage (AIM). FEBS Lett 2012; 586: 3569–3574
7. Joseph SB, Bradley MN, Castrillo A, Bruhn KW, Mak PA, Pei L et al. LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell 2004; 119: 299–309
8. Valledor AF, Hsu LC, Ogawa S, Sawka-Verhelle D, Karin M, Glass CK. Activation of liver X receptors and retinoid X receptors prevents bacterial-induced macrophage apoptosis. Proc Natl Acad Sci USA 2004; 101: 17813–17818
9. Arai S, Shelton JM, Chen M, Bradley MN, Castrillo A, Bookout AL et al. A role of the apoptosis inhibitory factor AIM/Sp/Api6 in atherosclerosis development. Cell Metab 2005; 1: 201–213
10. Hamada M, Nakamura M, Tran MT, Moriguchi T, Hong C, Ohsumi T et al. MafB promotes atherosclerosis by inhibiting foam-cell apoptosis. Nat Commun 2014; 5: 3147
11. Tissot JD, Sanchez JC, Vuadens F, Scherl A, Schifferli JA, Hochstrasser DF et al. IgM are associated to Sp alpha (CD5 antigen-like). Electrophoresis 2002; 23: 1203–1206
12. Kai T, Yamazaki T, Arai S, Miyazaki T. Stabilization and augmentation of circulating AIM in mice by synthesized IgM-Fc. PLoS One 2014; 9: e97037
13. Erlandsson L, Andersson K, Sigvardsson M, Lycke N, Leanderson T. Mice with an inactivated joining chain locus have perturbed IgM secretion. Eur J Immunol 1998; 28: 2355–2365
14. Boes M, Esau C, Fischer MB, Schmidt T, Carroll M, Chen J. Enhanced B-1 cell development, but impaired IgG antibody responses in mice deficient in secreted IgM. J Immunol 1998; 160: 4776–4787
15. Yamazaki S, Sugisawa R, Hiramoto E, Takai R, Matsumoto A, Senda Y et al. A proteolytic modification of AIM promotes its renal excretion. Sci Rep 2016; 6: 38762
16. Kurokawa J, Arai S, Nakashima K, Nishijima A, Miyake K, Ose R et al. AIM is endocytosed into adipocytes and decreases lipid droplets via inhibition of fatty acid synthase activity. Cell Metab 2010; 11: 479–492
17. Iwamura Y, Mori M, Nakashima K, Mikami T, Murayama K, Arai S et al. Apoptosis inhibitor of macrophage (AIM) diminishes lipid droplet-coating proteins leading to lipolysis in adipocytes. Biochem Biophys Res Commun 2012; 422: 476–481
18. Maehara N, Arai S, Mori M, Iwamura Y, Kurokawa J, Kai T et al. Circulating AIM prevents hepatocellular carcinoma through complement activation. Cell Rep 2014; 9: 61–74
19. Polo S, Pece S, Di Fiore PP. Endocytosis and cancer. Curr Opin Cell Biol 2004; 16: 156–161
20. Mosesson Y, Mills GB, Yarden Y. Derailed endocytosis: an emerging feature of cancer. Nat Rev Cancer 2008; 8: 835–850
21. Ozawa T, Maehara N, Kai T, Arai S, Miyazaki T. Dietary fructose-induced hepatocellular carcinoma development manifested in mice lacking apoptosis inhibitor of macrophage (AIM). Genes Cells 2016; 21: 1320–1332
22. Vera J, Fenutría R, Cañadas O, Figueras M, Mota R, Sarrias MR et al. The CD5 ectodomain interacts with conserved fungal cell wall components and protects from zymosan-induced septic shock-like syndrome. Proc Natl Acad Sci USA 2009; 106: 1506–1511
23. Miyazaki T, Arai S. A defense system against multiple diseases via biological garbage clearance mediated by soluble scavenger proteins. Inflamm Regen 2015; 35: 203–209
24. Henson PM, Vandivier RW, Douglas IS. Cell death, remodeling, and repair in chronic obstructive pulmonary disease? Proc Am Thorac Soc 2006; 3: 713–717
25. Sandahl M, Hunter DM, Strunk KE, Earp HS, Cook RS. Epithelial cell-directed efferocytosis in the post-partum mammary gland is necessary for tissue homeostasis and future lactation. BMC Dev Biol 2010; 10: 122
26. Juncadella IJ, Kadl A, Sharma AK, Shim YM, Hochreiter-Hufford A, Borish L et al. Apoptotic cell clearance by bronchial epithelial cells critically influences airway inflammation. Nature 2012; 493: 547–551
27. Wan E, Yeap XY, Dehn S, Terry R, Novak M, Zhang S et al. Enhanced efferocytosis of apoptotic cardiomyocytes through myeloid-epithelial-reproductive tyrosine kinase links acute inflammation resolution to cardiac repair after infarction. Circ Res 2013; 113: 1004–1012
28. Mochizuki A, Pace A, Rockwell CE, Roth KJ, Chow A, O'Brien KM et al. Hepatic stellate cells orchestrate clearance of necrotic cells in a hypoxia-inducible factor-1α-dependent manner by modulating macrophage phenotype in mice. J Immunol 2014; 192: 3847–3857
29. Amdur RL, Chawla LS, Amodeo S, Kimmel PL, Palant CE. Outcomes following diagnosis of acute renal failure in U.S. veterans: focus on acute tubular necrosis. Kidney Int 2009; 76: 1089–1097
30. Ishani A, Xue JL, Himmelfarb J, Eggers PW, Kimmel PL, Molitoris BA et al. Acute kidney injury increases risk of ESRD among elderly. J Am Soc Nephrol 2009; 20: 223–228
31. Bedford M, Farmer C, Levin A, Ali T, Stevens P. Acute kidney injury and CKD: chicken or egg? Am J Kidney Dis 2012; 59: 485–491
32. Susantitaphong P, Cruz DN, Cerda J, Abulfaraj M, Alqahtani F, Koulouridis I et al. World incidence of AKI: a meta-analysis. Clin J Am Soc Nephrol 2013; 8: 1482–1493
33. Molitoris BA. Therapeutic translation in acute kidney injury: the epithelial/endothelial axis. J Clin Invest 2014; 124: 2355–2363
34. Humphreys BD, Valerius MT, Kobayashi A, Mugford JW, Soeung S, Duffield JS et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2008; 2: 284–291
35. Bonventre JV, Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 2011; 121: 4210–4221
36. Kusaba T, Lalli M, Kramann R, Kobayashi A, Humphreys BD. Differentiated kidney epithelial cells repair injured proximal tubule. Proc Natl Acad Sci USA 2014; 111: 1527–1532
37. Arai S, Kitada K, Yamazaki T, Takai R, Zhang X, Tsugawa Y et al. Apoptosis inhibitor of macrophage protein enhances intraluminal debris clearance and ameliorates acute kidney injury in mice. Nat Med 2016; 22: 183–193
38. The American Veterinary Medical Foundation. Total Pet Ownership and Pet Populations. US Pet Ownership and Demographics Sourcebook, Section 1, 2012, American Veterinary Medical Association: Schaumburg, IL, USA
39. The European Pet Food Industry.Facts and Figures, 2014. Available at: http://www.fediaf.org/fileadmin/user_upload/Secretariat/facts_and_figures_2014.pdf
40. Lulich JP, O’Brien TD, Osborne CA, Polzin DJ. Feline renal failure: questions, answers, questions. Compend Contin Educ Pract Vet 1992; 14: 127–152
41. Brown SA. Linking treatment to staging in chronic kidney disease. Consultations in Feline Internal Medicine (edit. By August JR) 2010; 6: 475–482
42. White JD, Norris JM, Baral RM, Malik R. Naturally-occurring chronic renal disease in Australian cats: a prospective study of 184 cases. Aust Vet J 2006; 84: 188–194
43. White JD, Malik R, Norris JM. Feline chronic kidney disease: can we move from treatment to prevention? Vet J 2011; 190: 317–322
44. Sugisawa S, Hiramoto E, Matsuoka M, Iwai S, Takai R, Yamazaki T et al. Impact of feline AIM on the susceptibility of cats to renal disease. Sci Rep 2016; 6: 35251
45. Schmiedt CW, Brainard BM, Hinson W, Brown SA, Brown CA. Unilateral renal ischemia as a model of acute kidney injury and renal fibrosis in cats. Vet Pathol 2016; 53: 87–101
46. Gadjeva MG, Rouseva MM, Zlatarova AS, Reid KB, Kishore U, Kojouharova MS. Interaction of human C1q with IgG and IgM: revisited. Biochemistry 2008; 47: 13093–13102
47. Kantor AB, Herzenberg LA. Origin of murine B cell lineages. Annu Rev Immunol 1993; 11: 501–538
48. Hardy RR, Hayakawa K. CD5 B cells, a fetal B cell lineage. Adv Immunol 1994; 55: 297–339
49. Boes M. Role of natural and immune IgM antibodies in immune responses. Mol Immunol 2000; 37: 1141–1149
50. Pepys MB. Role of complement in the induction of immunological responses. Transplant Rev 1976; 32: 93–120
51. Ahearn JM, Fearon DT. Structure and function of the complement receptors, CR1 (CD35) and CR2 (CD21). Adv Immunol 1989; 46: 183–219
52. Heyman B. The immune complex: possible ways of regulating the antibody response. Immunol Today 1990; 11: 310–313
53. Carroll MC. The role of complement and complement receptors in induction and regulation of immunity. Annu Rev Immunol 1998; 16: 545–568
54. Allen CD, Cyster JG. Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Semin Immunol 2008; 20: 14–25
55. Honda S, Kurita N, Miyamoto A, Cho Y, Usui K, Takeshita K et al. Enhanced humoral immune responses against T-independent antigens in Fc alpha/muR-deficient mice. Proc Natl Acad Sci USA 2009; 106: 11230–11235
56. Shibuya A, Sakamoto N, Shimizu Y, Shibuya K, Osawa M, Hiroyama T et al. Fc alpha/mu receptor mediates endocytosis of IgM-coated microbes. Nat Immunol 2000; 1: 441–446
57. Kojima A, Iwata K, Seya T, Matsumoto M, Ariga H, Atkinson JP et al. Membrane cofactor protein (CD46) protects cells predominantly from alternative complement pathway-mediated C3-fragment deposition and cytolysis. J Immunol 1993; 151: 1519–1527
58. Medof ME, Kinoshita T, Nussenzweig V. Inhibition of complement activation on the surface of cells after incorporation of decay-accelerating factor (DAF) into their membranes. J Exp Med 1984; 160: 1558–1578
59. Miwa T, Song WC. Membrane complement regulatory proteins: insight from animal studies and relevance to human diseases. Int Immunopharmacol 2001; 1: 445–459
60. Rosenbloom AL. Obesity, insulin resistance, beta-cell autoimmunity, and the changing clinical epidemiology of childhood diabetes. Diabetes Care 2003; 26: 2954–2956
61. Hersoug LG, Linneberg A. The link between the epidemics of obesity and allergic diseases: does obesity induce decreased immune tolerance? Allergy 2007; 62: 1205–1213
62. Cambuli VM, Incani M, Cossu E, Congiu T, Scano F, Pilia S et al. Prevalence of type 1 diabetes autoantibodies (GADA, IA2, and IAA) in overweight and obese children. Diabetes Care 2010; 33: 820–822
63. Marzullo P, Minocci A, Tagliaferri MA, Guzzaloni G, Di Blasio A, De Medici C et al. 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 2010; 95: 3965–3972
64. Badaru A, Pihoker C. Type 2 diabetes in childhood: clinical characteristics and role of β-cell autoimmunity. Curr Diab Rep 2012; 12: 75–81
65. Winer DA, Winer S, Shen L, Wadia PP, Yantha J, Paltser G et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat Med 2011; 217: 610–617
66. MacLennan IC, Gray D, Kumararatne DS, Bazin H. The lymphocytes of splenic marginal zones: a distinct B-cell lineage. Immunol Today 1982; 3: 305–307
67. Lopes-Carvalho T, Kearney JF. Development and selection of marginal zone B cells. Immunol Rev 2004; 197: 192–205
68. Pillai S, Cariappa A, Moran ST. Marginal zone B cells. Annu Rev Immunol 2005; 23: 161–196
69. Oliver AM, Martin F, Kearney JF. IgMhighCD21high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J Immunol 1999; 162: 7198–7207
70. Meyer-Bahlburg A, Bandaranayake AD, Andrews SF, Rawlings DJ. Reduced c-myc expression levels limit follicular mature B cell cycling in response to TLR signals. J Immunol 2009; 182: 4065–4075
71. Li QZ, Xie C, Wu T, Mackay M, Aranow C, Putterman C et al. Identification of autoantibody clusters that best predict lupus disease activity using glomerular proteome arrays. J Clin Invest 2005; 115: 3428–3439
72. Li QZ, Zhou J, Wandstrat AE, Carr-Johnson F, Branch V, Karp DR et al. Protein array autoantibody profiles for insights into systemic lupus erythematosus and incomplete lupus syndromes. Clin Exp Immunol 2007; 147: 60–70
73. Li QZ, Zhou J, Lian Y, Zhang B, Branch VK, Carr-Johnson F et al. Interferon signature gene expression is correlated with autoantibody profiles in patients with incomplete lupus syndromes. Clin Exp Immunol 2010; 159: 281–291
74. Underhill GH, Minges-Wols HA, Fornek JL, Witte PL, Kansas GS. IgG plasma cells display a unique spectrum of leukocyte adhesion and homing molecules. Blood 2002; 99: 2905–2912
75. Halliwell RE. Autoimmune diseases in domestic animals. J Am Vet Med Assoc 1982; 181: 1088–1096
76. Martínez VG, Moestrup SK, Holmskov U, Mollenhauer J, Lozano F. The conserved scavenger receptor cysteine-rich superfamily in therapy and diagnosis. Pharmacol Rev 2011; 63: 967–1000
77. Sanjurjo L, Aran G, Roher N, Valledor AF, Sarrias MR. AIM/CD5L: a key protein in the control of immune homeostasis and inflammatory disease. J Leukoc Biol 2015; 98: 173–184
78. Miyazaki T, Kurokawa J, Arai S. AIMing at metabolic syndrome—towards the development of novel therapies for metabolic diseases via apoptosis inhibitor of macrophage (AIM). Circ J 2011; 75: 2522–2531
79. Shuai Z, Wang J, Badamagunta M, Choi J, Yang G, Zhang W et al. The fingerprint of antimitochondrial antibodies and the etiology of primary biliary cholangitis. Hepatology 2017; 65: 1670–1682
80. Hisamoto S, Shimoda S, Harada K, Iwasaka S, Onohara S, Chong Y et al. Hydrophobic bile acids suppress expression of AE2 in biliary epithelial cells and induce bile duct inflammation in primary biliary cholangitis. J Autoimmun 2016; 75: 150–160