A novel CD93 polymorphism in non-obese diabetic (NOD) and NZB/W F1 mice is linked to a CD4+ iNKT cell deficient state

Immunogenetics

Volumn 62, Issue 6, 2010, Pages 397-407

  Zekavat, Ghazal ^a   Mozaffari, Raha ^a   Arias, Vanessa J ^b   Rostami, Susan Y ^a   Badkerhanian, Armen ^a   Tenner, Andrea J ^b   Nichols, Kim E ^c   Naji, Ali ^a   Noorchashm, Hooman ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

CD93; Idd13; iNKT cells; Nkt2; NOD mice; NZB W F1 mice

Indexed keywords

AMINO ACID; CD93 PROTEIN; GENOMIC DNA; PROTEIN; UNCLASSIFIED DRUG; COMPLEMENT 1Q RECEPTOR; COMPLEMENT RECEPTOR; MEMBRANE PROTEIN;

ALLELE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL LYSATE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE SEQUENCE; GENETIC LINKAGE; GENETIC POLYMORPHISM; HOMEOSTASIS; MACROPHAGE; MOUSE; NATURAL KILLER T CELL; NEW ZEALAND BLACK MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRE B LYMPHOCYTE; PRIORITY JOURNAL; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CHROMOSOME MAP; GENETICS; IMMUNOLOGY; LYMPHOCYTE COUNT; MOLECULAR GENETICS; PHYSIOLOGY;

MURINAE; MUS;

ANIMALS; BASE SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CHROMOSOME MAPPING; LYMPHOCYTE COUNT; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, INBRED NZB; MOLECULAR SEQUENCE DATA; NATURAL KILLER T-CELLS; POLYMORPHISM, GENETIC; RECEPTORS, COMPLEMENT;

EID: 77953145250     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-010-0442-3     Document Type: Article

References (38)

1. AG Baxter SJ Kinder KJ Hammond R Scollay DI Godfrey 1997 Association between alphabetaTCR+CD4-CD8-T-cell deficiency and IDDM in NOD/Lt mice Diabetes 46 4 572 582 10.2337/diabetes.46.4.572 1:CAS:528:DyaK2sXitFKqsrY%3D 9075796
2. SS Bohlson R Silva MI Fonseca AJ Tenner 2005 CD93 is rapidly shed from the surface of human myeloid cells and the soluble form is detected in human plasma J Immunol 175 2 1239 1247 1:CAS:528:DC%2BD2MXlvFSjsr4%3D 16002728
3. JA Cain JA Smith JK Ondr B Wang JD Katz 2006 NKT cells and IFN-gamma establish the regulatory environment for the control of diabetogenic T cells in the nonobese diabetic mouse J Immunol 176 3 1645 1654 1:CAS:528: DC%2BD28XlsFynug%3D%3D 16424194
4. MP Cancro 2004 Peripheral B-cell maturation: the intersection of selection and homeostasis Immunol Rev 197 89 101 10.1111/j.0105-2896.2004.0099.x 1:CAS:528:DC%2BD2cXhs1Ghsbw%3D 14962189 (Pubitemid 38142170)
5. YG Chen JP Driver PA Silveira DV Serreze 2007 Subcongenic analysis of genetic basis for impaired development of invariant NKT cells in NOD mice Immunogenetics 59 9 705 712 10.1007/s00251-007-0236-4 1:CAS:528: DC%2BD2sXhtVCnsrvE 17619875 (Pubitemid 47415563)
6. S Chevrier C Genton A Kallies A Karnowski LA Otten B Malissen M Malissen M Botto LM Corcoran SL Nutt H Acha-Orbea 2009 CD93 is required for maintenance of antibody secretion and persistence of plasma cells in the bone marrow niche Proc Natl Acad Sci U S A 106 3895 3900 10.1073/pnas.0809736106 1:CAS:528:DC%2BD1MXjt1GksbY%3D 19228948
7. GH Danet JL Luongo G Butler MM Lu AJ Tenner MC Simon DA Bonnet 2002 C1qRp defines a new human stem cell population with hematopoietic and hepatic potential Proc Natl Acad Sci U S A 99 16 10441 10445 10.1073/pnas.162104799 1:CAS:528:DC%2BD38Xmt1Chsr4%3D 12140365
8. YD Dean EP McGreal P Gasque 2001 Endothelial cells, megakaryoblasts, platelets and alveolar epithelial cells express abundant levels of the mouse AA4 antigen, a C-type lectin-like receptor involved in homing activities and innate immune host defense Eur J Immunol 31 5 1370 1381 10.1002/1521-4141(200105)31: 5<1370::AID-IMMU1370>3.0.CO;2-B 1:CAS:528:DC%2BD3MXktVWjur0%3D 11465094 (Pubitemid 32454684)
9. N Duarte M Stenstrom S Campino ML Bergman M Lundholm D Holmberg SL Cardell 2004 Prevention of diabetes in nonobese diabetic mice mediated by CD1d-restricted nonclassical NKT cells J Immunol 173 5 3112 3118 1:CAS:528:DC%2BD2cXmvVCqsbk%3D 15322171
10. LM Esteban T Tsoutsman MA Jordan D Roach LD Poulton A Brooks OV Naidenko S Sidobre DI Godfrey AG Baxter 2003 Genetic control of NKT cell numbers maps to major diabetes and lupus loci J Immunol 171 6 2873 2878 1:CAS:528: DC%2BD3sXmvFGqt7w%3D 12960309
11. JM Fletcher MA Jordan SL Snelgrove RM Slattery FD Dufour K Kyparissoudis GS Besra DI Godfrey AG Baxter 2008 Congenic analysis of the NKT cell control gene Nkt2 implicates the peroxisomal protein Pxmp4 J Immunol 181 5 3400 3412 1:CAS:528:DC%2BD1cXhtVSiu7bO 18714012
12. MI Fonseca PM Carpenter M Park G Palmarini EL Nelson AJ Tenner 2001 C1qR(P), a myeloid cell receptor in blood, is predominantly expressed on endothelial cells in human tissue J Leukoc Biol 70 793 800 1:CAS:528: DC%2BD3MXosVKlsbs%3D 11698500
13. G Galli P Pittoni E Tonti C Malzone Y Uematsu M Tortoli D Maione G Volpini O Finco S Nuti S Tavarini P Dellabona R Rappuoli G Casorati S Abrignani 2007 Invariant NKT cells sustain specific B cell responses and memory Proc Natl Acad Sci U S A 104 10 3984 3989 10.1073/pnas.0700191104 1:CAS:528: DC%2BD2sXjt1ymu7c%3D 17360464 (Pubitemid 47181565)
14. DI Godfrey SJ Kinder P Silvera AG Baxter 1997 Flow cytometric study of T cell development in NOD mice reveals a deficiency in alphabetaTCR+CDR-CD8- thymocytes J Autoimmun 10 3 279 285 10.1006/jaut.1997.0129 1:STN:280: DyaK2szmtFOqtg%3D%3D 9218755 (Pubitemid 27286535)
15. KJ Hammond DG Pellicci LD Poulton OV Naidenko AA Scalzo AG Baxter DI Godfrey 2001 CD1d-restricted NKT cells: an interstrain comparison J Immunol 167 3 1164 1173 1:CAS:528:DC%2BD3MXls1WktLk%3D 11466330
16. MA Jordan J Fletcher AG Baxter 2004 Genetic control of NKT cell numbers Immunol Cell Biol 82 3 276 284 10.1111/j.0818-9641.2004.01264.x 1:CAS:528:DC%2BD2cXlvFemsb8%3D 15186259 (Pubitemid 38870022)
17. GS Kansas 1996 Selectins and their ligands: current concepts and controversies Blood 88 9 3259 3287 1:CAS:528:DyaK28XmsFKksL4%3D 8896391
18. TS Kim M Park RR Nepomuceno G Palmarini S Winokur CA Cotman U Bengtsson AJ Tenner 2000 Characterization of the murine homolog of C1qR(P): identical cellular expression pattern, chromosomal location and functional activity of the human and murine C1qR(P) Mol Immunol 37 7 377 389 10.1016/S0161-5890(00)00057-2 1:CAS:528:DC%2BD3cXosVCqs7s%3D 11074255
19. PB Langmuir MM Bridgett AL Bothwell IN Crispe 1993 Bone marrow abnormalities in the non-obese diabetic mouse Int Immunol 5 2 169 177 10.1093/intimm/5.2.169 1:CAS:528:DyaK2cXivFajtw%3D%3D 8452815
20. N Matsuki AK Stanic ME Embers L Van Kaer L Morel S Joyce 2003 Genetic dissection of V alpha 14J alpha 18 natural T cell number and function in autoimmune-prone mice J Immunol 170 11 5429 5437 1:CAS:528:DC%2BD3sXjvVynt7o%3D 12759418
21. JP McKearn C Baum JM Davie 1984 Cell surface antigens expressed by subsets of pre-B cells and B cells J Immunol 132 1 332 339 1:STN:280: DyaL2c%2FovV2jtw%3D%3D 6606670
22. RR Nepomuceno AJ Tenner 1998 C1qRP, the C1q receptor that enhances phagocytosis, is detected specifically in human cells of myeloid lineage, endothelial cells, and platelets J Immunol 160 4 1929 1935 1:CAS:528: DyaK1cXhtV2ntbk%3D 9469455
23. RR Nepomuceno AH Henschen-Edman WH Burgess AJ Tenner 1997 cDNA cloning and primary structure analysis of C1qR(P), the human C1q/MBL/SPA receptor that mediates enhanced phagocytosis in vitro Immunity 6 2 119 129 10.1016/S1074-7613(00)80419-7 1:CAS:528:DyaK2sXhsFajtbk%3D 9047234 (Pubitemid 27145557)
24. PJ Norsworthy PR Taylor MJ Walport M Botto 1999 Cloning of the mouse homolog of the 126-kDa human C1q/MBL/SP-A receptor, C1qR(p) Mamm Genome 10 8 789 793 10.1007/s003359901093 1:CAS:528:DyaK1MXkvV2msLo%3D 10430665 (Pubitemid 29390555)
25. PJ Norsworthy L Fossati-Jimack J Cortes-Hernandez PR Taylor AE Bygrave RD Thompson S Nourshargh MJ Walport M Botto 2004 Murine CD93 (C1qRp) contributes to the removal of apoptotic cells in vivo but is not required for C1q-mediated enhancement of phagocytosis J Immunol 172 6 3406 3414 1:CAS:528: DC%2BD2cXhvVKjtr8%3D 15004139
26. O Petrenko A Beavis M Klaine R Kittappa I Godin IR Lemischka 1999 The molecular characterization of the fetal stem cell marker AA4 Immunity 10 6 691 700 10.1016/S1074-7613(00)80068-0 1:CAS:528:DyaK1MXksVSmsb4%3D 10403644 (Pubitemid 29302922)
27. LD Poulton MJ Smyth CG Hawke P Silveira D Shepherd OV Naidenko DI Godfrey AG Baxter 2001 Cytometric and functional analyses of NK and NKT cell deficiencies in NOD mice Int Immunol 13 7 887 896 10.1093/intimm/13.7.887 1:CAS:528:DC%2BD3MXlsFOgtbs%3D 11431419
28. WJ Quinn 3rd N Noorchashm JE Crowley AJ Reed H Noorchashm A Naji MP Cancro 2006 Cutting edge: impaired transitional B cell production and selection in the nonobese diabetic mouse J Immunol 176 12 7159 7164 1:CAS:528: DC%2BD28Xlt1CltLY%3D 16751358
29. ZS Rahman SK Tin PN Buenaventura CH Ho EP Yap RY Yong DR Koh 2002 A novel susceptibility locus on chromosome 2 in the (New Zealand Black x New Zealand White)F1 hybrid mouse model of systemic lupus erythematosus J Immunol 168 6 3042 3049 1:CAS:528:DC%2BD38XitFSkurg%3D 11884477
30. AG Rolink J Andersson F Melchers 1998 Characterization of immature B cells by a novel monoclonal antibody, by turnover and by mitogen reactivity Eur J Immunol 28 11 3738 3748 10.1002/(SICI)1521-4141(199811)28:11<3738::AID- IMMU3738>3.0.CO;2-Q 1:CAS:528:DyaK1cXnsFKjs7o%3D 9842916 (Pubitemid 28510784)
31. SD Rosen 2004 Ligands for L-selectin: homing, inflammation, and beyond Annu Rev Immunol 22 129 156 10.1146/annurev.immunol.21.090501.080131 1:CAS:528:DC%2BD2cXktlOgs78%3D 15032576 (Pubitemid 38680420)
32. DV Serreze M Bridgett HD Chapman E Chen SD Richard EH Leiter 1998 Subcongenic analysis of the Idd13 locus in NOD/Lt mice: evidence for several susceptibility genes including a possible diabetogenic role for beta 2-microglobulin J Immunol 160 3 1472 1478 1:CAS:528:DyaK1cXnslemsw%3D%3D 9570569
33. PA Silveira ST Grey 2006 B cells in the spotlight: innocent bystanders or major players in the pathogenesis of type 1 diabetes Trends Endocrinol Metab 17 4 128 135 10.1016/j.tem.2006.03.006 1:CAS:528:DC%2BD28XksVOgsrY%3D 16580840
34. E Tonti G Galli C Malzone S Abrignani G Casorati P Dellabona 2009 NKT-cell help to B lymphocytes can occur independently of cognate interaction Blood 113 2 370 376 10.1182/blood-2008-06-166249 1:CAS:528: DC%2BD1MXptFSitQ%3D%3D 18832653
35. S Turley L Poirot M Hattori C Benoist D Mathis 2003 Physiological beta cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model J Exp Med 198 10 1527 1537 10.1084/jem.20030966 1:CAS:528:DC%2BD3sXptFOgsL4%3D 14623908 (Pubitemid 37467167)
36. MJ Wagner S Hussain M Mehan JM Verdi TL Delovitch 2005 A defect in lineage fate decision during fetal thymic invariant NKT cell development may regulate susceptibility to type 1 diabetes J Immunol 174 11 6764 6771 1:CAS:528:DC%2BD2MXkt1Omtr0%3D 15905517
37. SD Webster M Park MI Fonseca AJ Tenner 2000 Structural and functional evidence for microglial expression of C1qR(P), the C1q receptor that enhances phagocytosis J Leukoc Biol 67 1 109 116 1:CAS:528:DC%2BD3cXmt1Shsw%3D%3D 10648005
38. M Zhang SS Bohlson M Dy AJ Tenner 2005 Modulated interaction of the ERM protein, moesin, with CD93 Immunology 115 63 73 10.1111/j.1365-2567.2005.02120.x 1:CAS:528:DC%2BD2MXjvFaqt74%3D 15819698 (Pubitemid 40593292)