CCDC88B is a novel regulator of maturation and effector functions of T cells during pathological inflammation

Journal of Experimental Medicine

Volumn 211, Issue 13, 2014, Pages 2519-2535

  Kennedy, James M ^a   Fodil, Nassima ^a   Torre, Sabrina ^a   Bongfen, Silayuv E ^a   Olivier, Jean Frédéric ^a   Leung, Vicki ^a   Langlais, David ^a   Meunier, Charles ^a   Berghout, Joanne ^a   Langat, Pinky ^a   Schwartzentruber, Jeremy ^a   Majewski, Jacek ^a   Lathrop, Mark ^a   Vidal, Silvia M ^a   Gros, Philippe ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COILED COIL DOMAIN CONTAINING PROTEIN 88B; GAMMA INTERFERON; PROTEIN; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CARRIER PROTEIN; COILED-COIL DOMAIN CONTAINING 88B PROTEIN, MOUSE; ETHYLNITROSOUREA; LYMPHOCYTE ANTIGEN RECEPTOR; MESSENGER RNA;

ADULT; ANIMAL CELL; ARTICLE; AUTOIMMUNE DISEASE; BONE MARROW CELL; BRAIN MALARIA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIVISION; CELL MATURATION; CELL POPULATION; CELL TRANSFER; CYTOKINE PRODUCTION; EFFECTOR CELL; FEMALE; GENE MAPPING; GENETIC ASSOCIATION; HOMOZYGOSITY; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN PROCESSING; T LYMPHOCYTE; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; CELL DIFFERENTIATION; CHROMOSOME 11; CYTOLOGY; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; HEMATOPOIETIC SYSTEM; HUMAN; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE ACTIVATION; MALARIA, CEREBRAL; METABOLISM; MOLECULAR GENETICS; MUTANT MOUSE STRAIN; MUTATION; NUCLEOTIDE SEQUENCE; PARASITOLOGY; PATHOLOGY; PLASMODIUM BERGHEI;

ANIMALS; BASE SEQUENCE; CARRIER PROTEINS; CELL DIFFERENTIATION; CHROMOSOMES, HUMAN, PAIR 11; DISEASE RESISTANCE; ETHYLNITROSOUREA; FEMALE; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDIES; HEMATOPOIETIC SYSTEM; HUMANS; INFLAMMATION; LYMPHOCYTE ACTIVATION; MALARIA, CEREBRAL; MALE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MOLECULAR SEQUENCE DATA; MUTATION; MYELOID CELLS; ORGAN SPECIFICITY; PLASMODIUM BERGHEI; RECEPTORS, ANTIGEN, T-CELL; RNA, MESSENGER; T-LYMPHOCYTES;

EID: 84927646479     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20140455     Document Type: Article

References (65)

1. Barish, G.D., R.T. Yu, M. Karunasiri, C.B. Ocampo, J. Dixon, C. Benner, A.L. Dent, R.K. Tangirala, and R.M. Evans. 2010. Bcl-6 and NF-κB cistromes mediate opposing regulation of the innate immune response. Genes Dev. 24:2760-2765. http://dx.doi.org/10.1101/gad.1998010
2. Beecham, A.H., N.A. Patsopoulos, D.K. Xifara, M.F. Davis, A. Kemppinen, C. Cotsapas, T.S. Shah, C. Spencer, D. Booth, A. Goris, et al. International IBD Genetics Consortium (IIBDGC). 2013. Analysis of immune-related loci identifies 48 new susceptibility variants for multiple sclerosis. Nat. Genet. 45:1353-1360. http://dx.doi.org/10.1038/ng.2770
3. Berghout, J., D. Langlais, I. Radovanovic, M. Tam, J.D. MacMicking, M.M. Stevenson, and P. Gros. 2013. Irf8-regulated genomic responses drive pathological inflammation during cerebral malaria. PLoS Pathog. 9:e1003491. http://dx.doi.org/10.1371/journal.ppat.1003491
4. Bongfen, S.E., I.-G. Rodrigue-Gervais, J. Berghout, S. Torre, P. Cingolani, S.A. Wiltshire, G.A. Leiva-Torres, L. Letourneau, R. Sladek, M. Blanchette, et al. 2012. An N-ethyl-N-nitrosourea (ENU)-induced dominant negative mutation in the JAK3 kinase protects against cerebral malaria. PLoS ONE. 7:e31012. http://dx.doi.org/10.1371/journal.pone.0031012
5. Broman, K.W., H. Wu, S. Sen, and G.A. Churchill. 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics. 19:889-890. http://dx.doi.org/10.1093/bioinformatics/btg112
6. Brown, H., T.T. Hien, N. Day, N.T. Mai, L.V. Chuong, T.T. Chau, P.P. Loc, N.H. Phu, D. Bethell, J. Farrar, et al. 1999. Evidence of blood-brain barrier dysfunction in human cerebral malaria. Neuropathol. Appl. Neurobiol. 25:331-340. http://dx.doi.org/10.1046/j.1365-2990.1999.00188.x
7. Canonne-Hergaux, F., S. Gruenheid, P. Ponka, and P. Gros. 1999. Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron. Blood. 93:4406-4417.
8. Cho, B.K., C. Wang, S. Sugawa, H.N. Eisen, and J. Chen. 1999. Functional differences between memory and naive CD8 T cells. Proc. Natl. Acad. Sci. USA. 96:2976-2981. http://dx.doi.org/10.1073/pnas.96.6.2976
9. Cooper, J.D., D.J. Smyth, A.M. Smiles, V. Plagnol, N.M. Walker, J.E. Allen, K. Downes, J.C. Barrett, B.C. Healy, J.C. Mychaleckyj, et al. 2008. Metaanalysis of genome-wide association study data identifies additional type 1 diabetes risk loci. Nat. Genet. 40:1399-1401. http://dx.doi.org/10.1038/ng.249
10. de Souza, J.B., and E.M. Riley. 2002. Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes Infect. 4:291-300. http://dx.doi.org/10.1016/S1286-4579(02)01541-1
11. DeGrendele, H.C., P. Estess, and M.H. Siegelman. 1997. Requirement for CD44 in activated T cell extravasation into an inflammatory site. Science. 278:672-675. http://dx.doi.org/10.1126/science.278.5338.672
12. Dimas, A.S., S. Deutsch, B.E. Stranger, S.B. Montgomery, C. Borel, H. Attar-Cohen, C. Ingle, C. Beazley, M. Gutierrez Arcelus, M. Sekowska, et al. 2009. Common regulatory variation impacts gene expression in a cell type-dependent manner. Science. 325:1246-1250. http://dx.doi.org/10.1126/science.1174148
13. Fischer, A., B. Schmid, D. Ellinghaus, M. Nothnagel, K.I. Gaede, M. Schürmann, S. Lipinski, P. Rosenstiel, G. Zissel, K. Höhne, et al. 2012. A novel sarcoidosis risk locus for Europeans on chromosome 11q13.1. Am. J. Respir. Crit. Care Med. 186:877-885. http://dx.doi.org/10.1164/rccm.201204-0708OC
14. Gelfand, J.M., R.S. Stern, T. Nijsten, S.R. Feldman, J. Thomas, J. Kist, T. Rolstad, and D.J. Margolis. 2005. The prevalence of psoriasis in African Americans: results from a population-based study. J. Am. Acad. Dermatol. 52:23-26. http://dx.doi.org/10.1016/j.jaad.2004.07.045
15. Green, A., G. Brutti, C.C. Patterson, G. Dahlquist, G. Soltesz, A. Green, E. Schober, I. Weets, C. Vandevalle, F. Gorus, et al. EURODIAB ACE Study Group. 2000. Variation and trends in incidence of childhood diabetes in Europe. Lancet. 355:873-876. http://dx.doi.org/10.1016/S0140-6736(99)07125-1
16. Grundberg, E., K.S. Small, Å.K. Hedman, A.C. Nica, A. Buil, S. Keildson, J.T. Bell, T.-P. Yang, E. Meduri, A. Barrett, et al. Multiple Tissue Human Expression Resource (MuTHER) Consortium. 2012. Mapping cis- and trans-regulatory effects across multiple tissues in twins. Nat. Genet. 44:1084-1089. http://dx.doi.org/10.1038/ng.2394
17. Hansen, D.S. 2012. Inflammatory responses associated with the induction of cerebral malaria: lessons from experimental murine models. PLoS Pathog. 8:e1003045. http://dx.doi.org/10.1371/journal.ppat.1003045
18. Hansen, D.S., M.-A. Siomos, L. Buckingham, A.A. Scalzo, and L. Schofield. 2003. Regulation of murine cerebral malaria pathogenesis by CD1drestricted NKT cells and the natural killer complex. Immunity. 18:391-402. http://dx.doi.org/10.1016/S1074-7613(03)00052-9
19. Hansen, D.S., N.J. Bernard, C.Q. Nie, and L. Schofield. 2007. NK cells stimulate recruitment of CXCR3+ T cells to the brain during Plasmodium berghei-mediated cerebral malaria. J. Immunol. 178:5779-5788. http://dx.doi.org/10.4049/jimmunol.178.9.5779
20. Jostins, L., S. Ripke, R.K. Weersma, R.H. Duerr, D.P. McGovern, K.Y. Hui, J.C. Lee, L.P. Schumm, Y. Sharma, C.A. Anderson, et al. International IBD Genetics Consortium (IIBDGC). 2012. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 491:119-124. http://dx.doi.org/10.1038/nature11582
21. Juran, B.D., G.M. Hirschfield, P. Invernizzi, E.J. Atkinson, Y. Li, G. Xie, R. Kosoy, M. Ransom, Y. Sun, I. Bianchi, et al. Italian PBC Genetics Study Group. 2012. Immunochip analyses identify a novel risk locus for primary biliary cirrhosis at 13q14, multiple independent associations at four established risk loci and epistasis between 1p31 and 7q32 risk variants. Hum. Mol. Genet. 21:5209-5221. http://dx.doi.org/10.1093/hmg/dds359
22. Knoops, B., J. Goemaere, V. Van der Eecken, and J.-P. Declercq. 2011. Peroxiredoxin 5: structure, mechanism, and function of the mammalian atypical 2-Cys peroxiredoxin. Antioxid. Redox Signal. 15:817-829. http://dx.doi.org/10.1089/ars.2010.3584
23. Koch, M.W., L.M. Metz, and O. Kovalchuk. 2013. Epigenetic changes in patients with multiple sclerosis. Nat Rev Neurol. 9:35-43. http://dx.doi.org/10.1038/nrneurol.2012.226
24. Krieg, C., O. Boyman, Y.-X. Fu, and J. Kaye. 2007. B and T lymphocyte attenuator regulates CD8+ T cell-intrinsic homeostasis and memory cell generation. Nat. Immunol. 8:162-171. http://dx.doi.org/10.1038/ni1418
25. Lamb, T.J., D.E. Brown, A.J. Potocnik, and J. Langhorne. 2006. Insights into the immunopathogenesis of malaria using mouse models. Expert Rev. Mol. Med. 8:1-22. http://dx.doi.org/10.1017/S1462399406010581
26. Lawrence, T., D.A. Willoughby, and D.W. Gilroy. 2002. Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat. Rev. Immunol. 2:787-795. http://dx.doi.org/10.1038/nri915
27. Le-Niculescu, H., I. Niesman, T. Fischer, L. DeVries, and M.G. Farquhar. 2005. Identification and characterization of GIV, a novel Galpha i/s-interacting protein found on COPI, endoplasmic reticulum-Golgi transport vesicles. J. Biol. Chem. 280:22012-22020. http://dx.doi.org/10.1074/jbc. M501833200
28. Leighton, I.A., K.N. Dalby, F.B. Caudwell, P.T.W. Cohen, and P. Cohen. 1995. Comparison of the specificities of p70 S6 kinase and MAPKAP kinase-1 identifies a relatively specific substrate for p70 S6 kinase: the N-terminal kinase domain of MAPKAP kinase-1 is essential for peptide phosphorylation. FEBS Lett. 375:289-293. http://dx.doi.org/10.1016/0014-5793(95)01170-J
29. Li, H., and R. Durbin. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 25:1754-1760. http://dx.doi.org/10.1093/bioinformatics/btp324
30. Loftus, E.V. Jr. 2004. Clinical epidemiology of inflammatory bowel disease: Incidence, prevalence, and environmental influences. Gastroenterology. 126:1504-1517. http://dx.doi.org/10.1053/j.gastro.2004.01.063
31. Longley, R., C. Smith, A. Fortin, J. Berghout, B. McMorran, G. Burgio, S. Foote, and P. Gros. 2011. Host resistance to malaria: using mouse models to explore the host response. Mamm. Genome. 22:32-42. http://dx.doi.org/10.1007/s00335-010-9302-6
32. Majithia, V., and S.A. Geraci. 2007. Rheumatoid arthritis: diagnosis and management. Am. J. Med. 120:936-939. http://dx.doi.org/10.1016/j.amjmed.2007.04.005
33. Malone, C.J., L. Misner, N. Le Bot, M.-C. Tsai, J.M. Campbell, J. Ahringer, and J.G. White. 2003. The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell. 115:825-836. http://dx.doi.org/10.1016/S0092-8674(03)00985-1
34. Martin, J.-E., S. Assassi, L.-M. Diaz-Gallo, J.C. Broen, C.P. Simeon, I. Castellvi, E. Vicente-Rabaneda, V. Fonollosa, N. Ortego-Centeno, M.A. González-Gay, et al. BIOLUPUS. 2013. A systemic sclerosis and systemic lupus erythematosus pan-meta-GWAS reveals new shared susceptibility loci. Hum. Mol. Genet. 22:4021-4029. http://dx.doi.org/10.1093/hmg/ddt248
35. Matsushita, E., N. Asai, A. Enomoto, Y. Kawamoto, T. Kato, S. Mii, K. Maeda, R. Shibata, S. Hattori, M. Hagikura, et al. 2011. Protective role of Gipie, a Girdin family protein, in endoplasmic reticulum stress responses in endothelial cells. Mol. Biol. Cell. 22:736-747. http://dx.doi.org/10.1091/mbc. E10-08-0724
36. Miller, L.H., D.I. Baruch, K. Marsh, and O.K. Doumbo. 2002. The pathogenic basis of malaria. Nature. 415:673-679. http://dx.doi.org/10.1038/415673a
37. Mishra, S.K., and C.R.J.C. Newton. 2009. Diagnosis and management of the neurological complications of falciparum malaria. Nat Rev Neurol. 5:189-198. http://dx.doi.org/10.1038/nrneurol.2009.
38. Miyakoda, M., D. Kimura, M. Yuda, Y. Chinzei, Y. Shibata, K. Honma, and K. Yui. 2008. Malaria-specific and nonspecific activation of CD8+ T cells during blood stage of Plasmodium berghei infection. J. Immunol. 181:1420-1428. http://dx.doi.org/10.4049/jimmunol.181.2.1420
39. Newton, C.R., T.T. Hien, and N. White. 2000. Cerebral malaria. J. Neurol. Neurosurg. Psychiatry. 69:433-441. http://dx.doi.org/10.1136/jnnp.69.4.433
40. Ng, S.-L., B.A. Friedman, S. Schmid, J. Gertz, R.M. Myers, B.R. Tenoever, and T. Maniatis. 2011. IκB kinase epsilon (IKKε) regulates the balance between type I and type II interferon responses. Proc. Natl. Acad. Sci. USA. 108:21170-21175. http://dx.doi.org/10.1073/pnas.1119137109
41. Nica, A.C., L. Parts, D. Glass, J. Nisbet, A. Barrett, M. Sekowska, M. Travers, S. Potter, E. Grundberg, K. Small, et al. MuTHER Consortium. 2011. The architecture of gene regulatory variation across multiple human tissues: the MuTHER study. PLoS Genet. 7:e1002003. http://dx.doi.org/10.1371/journal.pgen.1002003
42. Nitcheu, J., O. Bonduelle, C. Combadiere, M. Tefit, D. Seilhean, D. Mazier, and B. Combadiere. 2003. Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis. J. Immunol. 170:2221-2228. http://dx.doi.org/10.4049/jimmunol.170.4.2221
43. Oshita, A., S. Kishida, H. Kobayashi, T. Michiue, T. Asahara, M. Asashima, and A. Kikuchi. 2003. Identification and characterization of a novel Dvlbinding protein that suppresses Wnt signalling pathway. Genes Cells. 8:1005-1017. http://dx.doi.org/10.1111/j.1365-2443.2003.00692.x
44. Petukhova, L., M. Duvic, M. Hordinsky, D. Norris, V. Price, Y. Shimomura, H. Kim, P. Singh, A. Lee, W.V. Chen, et al. 2010. Genome-wide association study in alopecia areata implicates both innate and adaptive immunity. Nature. 466:113-117. http://dx.doi.org/10.1038/nature09114
45. Porcherie, A., C. Mathieu, R. Peronet, E. Schneider, J. Claver, P.-H. Commere, H. Kiefer-Biasizzo, H. Karasuyama, G. Milon, M. Dy, et al. 2011. Critical role of the neutrophil-associated high-affinity receptor for IgE in the pathogenesis of experimental cerebral malaria. J. Exp. Med. 208:2225-2236. http://dx.doi.org/10.1084/jem.20110845
46. Quinlan, A.R., and I.M. Hall. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 26:841-842. http://dx.doi.org/10.1093/bioinformatics/btq033
47. Rahman, A., and D.A. Isenberg. 2008. Systemic lupus erythematosus. N. Engl. J. Med. 358:929-939. http://dx.doi.org/10.1056/NEJMra071297
48. Ramagopalan, S.V., R. Dobson, U.C. Meier, and G. Giovannoni. 2010. Multiple sclerosis: risk factors, prodromes, and potential causal pathways. Lancet Neurol. 9:727-739. http://dx.doi.org/10.1016/S1474-4422(10)70094-6
49. Raychaudhuri, S., E.F. Remmers, A.T. Lee, R. Hackett, C. Guiducci, N.P. Burtt, L. Gianniny, B.D. Korman, L. Padyukov, F.A.S. Kurreeman, et al. 2008. Common variants at CD40 and other loci confer risk of rheumatoid arthritis. Nat. Genet. 40:1216-1223. http://dx.doi.org/10.1038/ng.233
50. Rénia, L., S.M. Potter, M. Mauduit, D.S. Rosa, M. Kayibanda, J.-C. Deschemin, G. Snounou, and A.C. Grüner. 2006. Pathogenic T cells in cerebral malaria. Int. J. Parasitol. 36:547-554. http://dx.doi.org/10.1016/j.ijpara.2006.02.007
51. Richer, E., S.T. Qureshi, S.M. Vidal, and D. Malo. 2008. Chemical mutagenesis: a new strategy against the global threat of infectious diseases. Mamm. Genome. 19:309-317. http://dx.doi.org/10.1007/s00335-008-9114-0
52. Richer, E., C. Prendergast, and D.E. Zhang. 2010. N-ethyl-N-nitrosourea- induced mutation in ubiquitin-specific peptidase 18 causes hyperactivation of IFN-αβ signaling and suppresses STAT4-induced IFN-γ production, resulting in increased susceptibility to Salmonella typhimurium. J. Immunol. 185:3593-3601. http://dx.doi.org/10.4049/jimmunol.1000890
53. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22:745-763. http://dx.doi.org/10.1146/annurev. immunol.22.012703.104702
54. Serhan, C.N., P.A. Ward, and D.W. Gilroy. 2010. Fundamentals of Inflammation. Cambridge University Press. Cambridge, England, UK.
55. Simpson, F., S. Martin, T.M. Evans, M. Kerr, D.E. James, R.G. Parton, R.D. Teasdale, and C. Wicking. 2005. A novel hook-related protein family and the characterization of hook-related protein 1. Traffic. 6:442-458. http://dx.doi.org/10.1111/j.1600-0854.2005.00289.x
56. Strange, A., F. Capon, C.C.A. Spencer, J. Knight, M.E. Weale, M.H. Allen, A. Barton, G. Band, C. Bellenguez, J.G.M. Bergboer, et al. Genetic Analysis of Psoriasis Consortium & the Wellcome Trust Case Control Consortium 2. 2010. A genome-wide association study identifies new psoriasis susceptibility loci and an interaction between HLA-C and ERAP1. Nat. Genet. 42:985-990. http://dx.doi.org/10.1038/ng.694
57. Sun, H.-N., S.-U. Kim, S.M. Huang, J.-M. Kim, Y.-H. Park, S.-H. Kim, H.-Y. Yang, K.-J. Chung, T.-H. Lee, H.S. Choi, et al. 2010. Microglial peroxiredoxin V acts as an inducible anti-inflammatory antioxidant through cooperation with redox signaling cascades. J. Neurochem. 114:39-50.
58. Trynka, G., K.A. Hunt, N.A. Bockett, J. Romanos, V. Mistry, A. Szperl, S.F. Bakker, M.T. Bardella, L. Bhaw-Rosun, G. Castillejo, et al. Wellcome Trust Case Control Consortium (WTCCC). 2011. Dense genotyping identifies and localizes multiple common and rare variant association signals in celiac disease. Nat. Genet. 43:1193-1201. http://dx.doi.org/10.1038/ng.998
59. Tsoi, L.C., S.L. Spain, J. Knight, E. Ellinghaus, P.E. Stuart, F. Capon, J. Ding, Y. Li, T. Tejasvi, J.E. Gudjonsson, et al. Wellcome Trust Case Control Consortium 2. 2012. Identification of 15 new psoriasis susceptibility loci highlights the role of innate immunity. Nat. Genet. 44:1341-1348. http://dx.doi.org/10.1038/ng.2467
60. Veiga-Fernandes, H., U. Walter, C. Bourgeois, A. McLean, and B. Rocha. 2000. Response of naïve and memory CD8+ T cells to antigen stimulation in vivo. Nat. Immunol. 1:47-53. http://dx.doi.org/10.1038/76907
61. Villegas-Mendez, A., R. Greig, T.N. Shaw, J.B. de Souza, E. Gwyer Findlay, J.S. Stumhofer, J.C.R. Hafalla, D.G. Blount, C.A. Hunter, E.M. Riley, and K.N. Couper. 2012. IFN-γ-producing CD4+ T cells promote experimental cerebral malaria by modulating CD8+ T cell accumulation within the brain. J. Immunol. 189:968-979. http://dx.doi.org/10.4049/jimmunol.1200688
62. Walenta, J.H., A.J. Didier, X. Liu, and H. Krämer. 2001. The Golgi-associated hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell Biol. 152:923-934. http://dx.doi.org/10.1083/jcb.152.5.923
63. Wang, K., M. Li, and H. Hakonarson. 2010. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38:e164. http://dx.doi.org/10.1093/nar/gkq603
64. Wang, M.H., C. Fiocchi, X. Zhu, S. Ripke, M.I. Kamboh, N. Rebert, R.H. Duerr, and J.P. Achkar. 2014. Gene-gene and gene-environment interactions in ulcerative colitis. Hum. Genet. 133:547-558. http://dx.doi.org/10.1007/s00439-013-1395-z
65. Yañez, D.M., D.D. Manning, A.J. Cooley, W.P. Weidanz, and H.C. van der Heyde. 1996. Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J. Immunol. 157:1620-1624.