Shark class II invariant chain reveals ancient conserved relationships with cathepsins and MHC class II

Developmental and Comparative Immunology

Volumn 36, Issue 3, 2012, Pages 521-533

  Criscitiello, Michael F ^a   Ohta, Yuko ^b   Graham, Matthew D ^b   Eubanks, Jeannine O ^a   Chen, Patricia L ^a   Flajnik, Martin F ^b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Antigen processing; Evolution; Invariant chain; MHC; Shark

Indexed keywords

CATHEPSIN; HETERODIMER; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RNA;

ADAPTIVE IMMUNITY; ALTERNATIVE RNA SPLICING; ANTIGEN PRESENTING CELL; ARTICLE; CONTROLLED STUDY; FISH; GENE DUPLICATION; GENE EXPRESSION; GENE FUNCTION; GENE STRUCTURE; GENETIC CONSERVATION; GENETIC VARIABILITY; LIZARD; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; SHARK;

AGNATHA; CHONDRICHTHYES; CHORDATA; GINGLYMOSTOMATIDAE; OSTEICHTHYES; SQUAMATA; TELEOSTEI; VERTEBRATA;

EID: 84855838748     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2011.09.008     Document Type: Article

References (83)

1. Ashman J.B., Miller J. A role for the transmembrane domain in the trimerization of the MHC class II-associated invariant chain. J. Immunol. 1999, 163:2704-2712.
2. Bajoghli B., Guo P., Aghaallaei N., Hirano M., Strohmeier C., McCurley N., Bockman D.E., Schorpp M., Cooper M.D., Boehm T. A thymus candidate in lampreys. Nature 2011, 470:90-94.
3. Bakke O., Dobberstein B. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 1990, 63:707-716.
4. Bartl S., Baish M.A., Flajnik M.F., Ohta Y. Identification of class I genes in cartilaginous fish, the most ancient group of vertebrates displaying an adaptive immune response. J. Immunol. 1997, 159:6097-6104.
5. Bernstein R.M., Schluter S.F., Lake D.F., Marchalonis J.J. Evolutionary conservation and molecular-cloning of the recombinase activating gene-1. Biochem. Biophys. Res. Co. 1994, 205:687-692.
6. Bevec T., Stoka V., Pungercic G., Dolenc I., Turk V. Major histocompatibility complex class II-associated p41 invariant chain fragment is a strong inhibitor of lysosomal cathepsin L. J. Exp. Med. 1996, 183:1331-1338.
7. Bijlmakers M.J., Benaroch P., Ploegh H.L. Mapping functional regions in the lumenal domain of the class II-associated invariant chain. J. Exp. Med. 1994, 180:623-629.
8. 4+ T cell selection in mice lacking invariant chain expression. J. Exp. Med. 1993, 177:1699-1712.
9. Bikoff E.K., Kenty G., Van Kaer L. Distinct peptide loading pathways for MHC class II molecules associated with alternative Ii chain isoforms. J. Immunol. 1998, 160:3101-3110.
10. Blander J.M., Medzhitov R. On regulation of phagosome maturation and antigen presentation. Nat. Immunol. 2006, 7:1029-1035.
11. Blum J.S., Cresswell P. Role for intracellular proteases in the processing and transport of class II HLA antigens. Proc. Natl. Acad. Sci. USA 1988, 85:3975-3979.
12. Brown A.M., Wright K.L., Ting J.P. Human major histocompatibility complex class II-associated invariant chain gene promoter. Functional analysis and in vivo protein/DNA interactions of constitutive and IFN-gamma-induced expression. J. Biol. Chem. 1993, 268:26328-26333.
13. Brown W.M., Dziegielewska K.M. Friends and relations of the cystatin superfamily - new members and their evolution. Protein Sci. 1997, 6:5-12.
14. Chapman H.A. Endosomal proteolysis and MHC class II function. Curr. Opin. Immunol. 1998, 10:93-102.
15. Conticello S.G., Thomas C.J., Petersen-Mahrt S.K., Neuberger M.S. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol. Biol. Evol. 2005, 22:367-377.
16. Coulombe R., Grochulski P., Sivaraman J., Menard R., Mort J.S., Cygler M. Structure of human procathepsin L reveals the molecular basis of inhibition by the prosegment. EMBO J. 1996, 15:5492-5503.
17. Criscitiello M.F., Flajnik M.F. Four primordial immunoglobulin light chain isotypes, including lambda and kappa, identified in the most primitive living jawed vertebrates. Eur. J. Immunol. 2007, 37:2683-2694.
18. Criscitiello M.F., Kamper S.M., McKinney E.C. Allelic polymorphism of TCRalpha chain constant domain genes in the bicolor damselfish. Dev. Comp. Immunol. 2004, 28:781-792.
19. Criscitiello M.F., Ohta Y., Saltis M., McKinney E.C., Flajnik M.F. Evolutionarily conserved TCR binding sites, identification of T cells in primary lymphoid tissues, and surprising trans-rearrangements in nurse shark. J. Immunol. 2010, 184:6950-6960.
20. Criscitiello M.F., Saltis M., Flajnik M.F. An evolutionarily mobile antigen receptor variable region gene: doubly rearranging NAR-TcR genes in sharks. Proc. Natl. Acad. Sci. USA 2006, 103:5036-5041.
21. Dijkstra J.M., Kiryu I., Kollner B., Yoshiura Y., Ototake M. MHC class II invariant chain homologues in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 2003, 15:91-105.
22. Dixon A.M., Stanley B.J., Matthews E.E., Dawson J.P., Engelman D.M. Invariant chain transmembrane domain trimerization: a step in MHC class II assembly. Biochemistry 2006, 45:5228-5234.
23. Flajnik M.F. Comparative analyses of immunoglobulin genes: surprises and portents. Nat. Rev. Immunol. 2002, 2:688-698.
24. Flajnik M.F., Kasahara M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat. Rev. Genet. 2010, 11:47-59.
25. Freisewinkel I.M., Schenck K., Koch N. The segment of invariant chain that is critical for association with major histocompatibility complex class II molecules contains the sequence of a peptide eluted from class II polypeptides. Proc. Natl. Acad. Sci. USA 1993, 90:9703-9706.
26. Fujiki K., Smith C.M., Liu L., Sundick R.S., Dixon B. Alternate forms of MHC class II-associated invariant chain are not produced by alternative splicing in rainbow trout (Oncorhynchus mykiss) but are encoded by separate genes. Dev. Comp. Immunol. 2003, 27:377-391.
27. Ghosh P., Amaya M., Mellins E., Wiley D.C. The structure of an intermediate in class II MHC maturation: CLIP bound to HLA-DR3. Nature 1995, 378:457-462.
28. Guncar G., Pungercic G., Klemencic I., Turk V., Turk D. Crystal structure of MHC class II-associated p41 Ii fragment bound to cathepsin L reveals the structural basis for differentiation between cathepsins L and S. EMBO J. 1999, 18:793-803.
29. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp. Ser. 1999, 41:95-98.
30. Jasanoff A., Wagner G., Wiley D.C. Structure of a trimeric domain of the MHC class II-associated chaperonin and targeting protein Ii. EMBO J. 1998, 17:6812-6818.
31. Jones P.P., Murphy D.B., Hewgill D., McDevitt H.O. Detection of a common polypeptide chain in I-A and I-E sub-region immunoprecipitates. Mol. Immunol. 1979, 16:51-60.
32. Kasahara M., Vazquez M., Sato K., McKinney E.C., Flajnik M.F. Evolution of the major histocompatibility complex: isolation of class II A cDNA clones from the cartilaginous fish. Proc. Natl. Acad. Sci. USA 1992, 89:6688-6692.
33. Katunuma N., Kakegawa H., Matsunaga Y., Saibara T. Immunological significances of invariant chain from the aspect of its structural homology with the cystatin family. FEBS Lett. 1994, 349:265-269.
34. Koch N., Moldenhauer G., Hofmann W.J., Moller P. Rapid intracellular pathway gives rise to cell surface expression of the MHC class II-associated invariant chain (CD74). J. Immunol. 1991, 147:2643-2651.
35. Kongsvik T.L., Honing S., Bakke O., Rodionov D.G. Mechanism of interaction between leucine-based sorting signals from the invariant chain and clathrin-associated adaptor protein complexes AP1 and AP2. J. Biol. Chem. 2002, 277:16484-16488.
36. Lamb C.A., Cresswell P. Assembly and transport properties of invariant chain trimers and HLA-DR-invariant chain complexes. J. Immunol. 1992, 148:3478-3482.
37. Lenarcic B., Bevec T. Thyropins - new structurally related proteinase inhibitors. Biol. Chem. 1998, 379:105-111.
38. Leng L., Metz C.N., Fang Y., Xu J., Donnelly S., Baugh J., Delohery T., Chen Y., Mitchell R.A., Bucala R. MIF signal transduction initiated by binding to CD74. J. Exp. Med. 2003, 197:1467-1476.
39. Leong J.S., Jantzen S.G., von Schalburg K.R., Cooper G.A., Messmer A.M., Liao N.Y., Munro S., Moore R., Holt R.A., Jones S.J., Davidson W.S., Koop B.F. Salmo salar and Esox lucius full-length cDNA sequences reveal changes in evolutionary pressures on a post-tetraploidization genome. BMC Genom. 2010, 11:279.
40. Lombardi G., Burzyn D., Mundinano J., Berguer P., Bekinschtein P., Costa H., Castillo L.F., Goldman A., Meiss R., Piazzon I., Nepomnaschy I. Cathepsin-L influences the expression of extracellular matrix in lymphoid organs and plays a role in the regulation of thymic output and of peripheral T cell number. J. Immunol. 2005, 174:7022-7032.
41. Long E.O., Strubin M., Wake C.T., Gross N., Carrel S., Goodfellow P., Accolla R.S., Mach B. Isolation of cDNA clones for the p33 invariant chain associated with HLA-DR antigens. Proc. Natl. Acad. Sci. USA 1983, 80:5714-5718.
42. Lundin L.G., Larhammar D., Hallbook F. Numerous groups of chromosomal regional paralogies strongly indicate two genome doublings at the root of the vertebrates. J. Struct. Func. Genom. 2003, 3:53-63.
43. Malcherek G., Gnau V., Jung G., Rammensee H.G., Melms A. Supermotifs enable natural invariant chain-derived peptides to interact with many major histocompatibility complex-class II molecules. J. Exp. Med. 1995, 181:527-536.
44. Matza D., Kerem A., Medvedovsky H., Lantner F., Shachar I. Invariant chain-induced B cell differentiation requires intramembrane proteolytic release of the cytosolic domain. Immunity 2002, 17:549-560.
45. Matza D., Lantner F., Bogoch Y., Flaishon L., Hershkoviz R., Shachar I. Invariant chain induces B cell maturation in a process that is independent of its chaperonic activity. Proc. Natl. Acad. Sci. USA 2002, 99:3018-3023.
46. Mihelic M., Turk D. Two decades of thyroglobulin type-1 domain research. Biol. Chem. 2007, 388:1123-1130.
47. Nair S.V., Del Valle H., Gross P.S., Terwilliger D.P., Smith L.C. Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiol. Genom. 2005, 22:33-47.
48. Nakagawa T., Roth W., Wong P., Nelson A., Farr A., Deussing J., Villadangos J.A., Ploegh H., Peters C., Rudensky A.Y. Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 1998, 280:450-453.
49. Neefjes J.J., Ploegh H.L. Inhibition of endosomal proteolytic activity by leupeptin blocks surface expression of MHC class II molecules and their conversion to SDS resistance alpha beta heterodimers in endosomes. EMBO J. 1992, 11:411-416.
50. O'Sullivan D.M., Noonan D., Quaranta V. Four Ia invariant chain forms derive from a single gene by alternate splicing and alternate initiation of transcription/translation. J. Exp. Med. 1987, 166:444-460.
51. Ohta Y., Landis E., Boulay T., Phillips R.B., Collet B., Secombes C.J., Flajnik M.F., Hansen J.D. Homologs of CD83 from elasmobranch and teleost fish. J. Immunol. 2004, 173:4553-4560.
52. Ohta Y., McKinney E.C., Criscitiello M.F., Flajnik M.F. Proteasome, transporter associated with antigen processing, and class I genes in the nurse shark Ginglymostoma cirratum: evidence for a stable class I region and MHC haplotype lineages. J. Immunol. 2002, 168:771-781.
53. Ohta Y., Shiina T., Lohr R.L., Hosomichi K., Pollin T.I., Heist E.J., Suzuki S., Inoko H., Flajnik M.F. Primordial linkage of beta2-microglobulin to the MHC. J. Immunol. 2011, 186:3563-3571.
54. Pancer Z., Saha N.R., Kasamatsu J., Suzuki T., Amemiya C.T., Kasahara M., Cooper M.D. Variable lymphocyte receptors in hagfish. Proc. Natl. Acad. Sci. USA 2005, 102(26):9224-9229.
55. Parra Z.E., Ohta Y., Criscitiello M.F., Flajnik M.F., Miller R.D. The dynamic TCRdelta: TCRdelta chains in the amphibian Xenopus tropicalis utilize antibody-like V genes. Eur. J. Immunol. 2010, 40:2319-2329.
56. Paul P., van den Hoorn T., Jongsma M.L., Bakker M.J., Hengeveld R., Janssen L., Cresswell P., Egan D.A., van Ham M., Ten Brinke A., Ovaa H., Beijersbergen R.L., Kuijl C., Neefjes J. A Genome-wide multidimensional RNAi screen reveals pathways controlling MHC class II antigen presentation. Cell 2011, 145:268-283.
57. Pieters J., Bakke O., Dobberstein B. The MHC class II-associated invariant chain contains two endosomal targeting signals within its cytoplasmic tail. J. Cell Sci. 1993, 106(Pt 3):831-846.
58. Pond L., Kuhn L.A., Teyton L., Schutze M.P., Tainer J.A., Jackson M.R., Peterson P.A. A role for acidic residues in di-leucine motif-based targeting to the endocytic pathway. J. Biol. Chem. 1995, 270:19989-19997.
59. Rast J.P., Anderson M.K., Strong S.J., Luer C., Litman R.T., Litman G.W. Alpha, beta, gamma, and delta T cell antigen receptor genes arose early in vertebrate phylogeny. Immunity 1997, 6:1-11.
60. Riese R.J., Chapman H.A. Cathepsins and compartmentalization in antigen presentation. Curr. Opin. Immunol. 2000, 12:107-113.
61. Rogozin I.B., Iyer L.M., Liang L., Glazko G.V., Liston V.G., Pavlov Y.I., Aravind L., Pancer Z. Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nat. Immunol. 2007, 8:647-656.
62. Romagnoli P., Germain R.N. The CLIP region of invariant chain plays a critical role in regulating major histocompatibility complex class II folding, transport, and peptide occupancy. J. Exp. Med. 1994, 180:1107-1113.
63. Saha N.R., Smith J., Amemiya C.T. Evolution of adaptive immune recognition in jawless vertebrates. Semin. Immunol. 2010, 22:25-33.
64. Schafer P.H., Green J.M., Malapati S., Gu L., Pierce S.K. HLA-DM is present in one-fifth the amount of HLA-DR in the class II peptide-loading compartment where it associates with leupeptin-induced peptide (LIP)-HLA-DR complexes. J. Immunol. 1996, 157:5487-5495.
65. Schutze M.P., Peterson P.A., Jackson M.R. An N-terminal double-arginine motif maintains type II membrane proteins in the endoplasmic reticulum. EMBO J. 1994, 13:1696-1705.
66. Schwarz R., Dayhoff M. Matrices for detecting distant relationships. Atlas of Protein Sequences 1979, 353-358. National Biomedical Research Foundation. D. M (Ed.).
67. Sevenich L., Hagemann S., Stoeckle C., Tolosa E., Peters C., Reinheckel T. Expression of human cathepsin L or human cathepsin V in mouse thymus mediates positive selection of T helper cells in cathepsin L knock-out mice. Biochimie 2010, 92:1674-1680.
68. Shachar I., Elliott E.A., Chasnoff B., Grewal I.S., Flavell R.A. Reconstitution of invariant chain function in transgenic mice in vivo by individual p31 and p41 isoforms. Immunity 1995, 3:373-383.
69. Shi X., Leng L., Wang T., Wang W., Du X., Li J., McDonald C., Chen Z., Murphy J.W., Lolis E., Noble P., Knudson W., Bucala R. CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 2006, 25:595-606.
70. Silva D.S., Reis M.I., Nascimento D.S., do Vale A., Pereira P.J., dos Santos N.M. Sea bass (Dicentrarchus labrax) invariant chain and class II major histocompatibility complex: sequencing and structural analysis using 3D homology modelling. Mol. Immunol. 2007, 44:3758-3776.
71. Star B., Nederbragt A.J., Jentoft S., Grimholt U., Malmstrom M., Gregers T.F., Rounge T.B., Paulsen J., Solbakken M.H., Sharma A., Wetten O.F., Lanzen A., Winer R., Knight J., Vogel J.H., Aken B., Andersen O., Lagesen K., Tooming-Klunderud A., Edvardsen R.B., Tina K.G., Espelund M., Nepal C., Previti C., Karlsen B.O., Moum T., Skage M., Berg P.R., Gjoen T., Kuhl H., Thorsen J., Malde K., Reinhardt R., Du L., Johansen S.D., Searle S., Lien S., Nilsen F., Jonassen I., Omholt S.W., Stenseth N.C., Jakobsen K.S. The genome sequence of Atlantic cod reveals a unique immune system. Nature 2011, 477(7363):207-210.
72. Strubin M., Berte C., Mach B. Alternative splicing and alternative initiation of translation explain the four forms of the Ia antigen-associated invariant chain. EMBO J. 1986, 5:3483-3488.
73. Takaesu N.T., Lower J.A., Robertson E.J., Bikoff E.K. Major histocompatibility class II peptide occupancy, antigen presentation, and CD4+ T cell function in mice lacking the p41 isoform of invariant chain. Immunity 1995, 3:385-396.
74. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
75. Ting J.P., Trowsdale J. Genetic control of MHC class II expression. Cell 2002, 109(Suppl.):S21-S33.
76. Turk D., Guncar G., Turk V. The p41 fragment story. IUBMB Life 1999, 48:7-12.
77. Turk V., Turk B., Turk D. Lysosomal cysteine proteases: facts and opportunities. EMBO J. 2001, 20:4629-4633.
78. Uinuk-Ool T.S., Takezaki N., Kuroda N., Figueroa F., Sato A., Samonte I.E., Mayer W.E., Klein J. Phylogeny of antigen-processing enzymes: cathepsins of a cephalochordate, an agnathan and a bony fish. Scand. J. Immunol. 2003, 58:436-448.
79. Viville S., Neefjes J., Lotteau V., Dierich A., Lemeur M., Ploegh H., Benoist C., Mathis D. Mice lacking the MHC class II-associated invariant chain. Cell 1993, 72:635-648.
80. Wahle E., Keller W. The biochemistry of 3'-end cleavage and polyadenylation of messenger RNA precursors. Ann. Rev. Biochem. 1992, 61:419-440.
81. Ye Q., Finn P.W., Sweeney R., Bikoff E.K., Riese R.J. MHC class II-associated invariant chain isoforms regulate pulmonary immune responses. J. Immunol. 2003, 170:1473-1480.
82. Yoder J.A., Haire R.N., Litman G.W. Cloning of two zebrafish cDNAs that share domains with the MHC class II-associated invariant chain. Immunogenetics 1999, 50:84-88.
83. Zhong G., Castellino F., Romagnoli P., Germain R.N. Evidence that binding site occupancy is necessary and sufficient for effective major histocompatibility complex (MHC) class II transport through the secretory pathway redefines the primary function of class II-associated invariant chain peptides (CLIP). J. Exp. Med. 1996, 184:2061-2066.