Glycans as key checkpoints of T cell activity and function

Frontiers in Immunology

Volumn 9, Issue NOV, 2018, Pages

  Pereira, Márcia S ^a,b   Alves, Inês ^a,b,c   Vicente, Manuel ^a,b   Campar, Ana ^a,b,d   Silva, Mariana C ^a,b   Padrão, Nuno A ^a,b,c   Pinto, Vanda ^a,b   Fernandes, Ångela ^a,b   Dias, Ana M ^a,b   Pinho, Salomé S ^a,b,c  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c University of Porto   (Portugal)

^d Centro Hospitalar Universitario do Porto   (Portugal)

Author keywords

Autoimmunity; Glycans; Immune response; N glycosylation; Self tolerance; T cells

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GALECTIN 1; GAMMA INTERFERON; GLYCAN; LEUKOSIALIN; MYC PROTEIN; N ACETYLGLUCOSAMINE; NOTCH RECEPTOR; P SELECTIN GLYCOPROTEIN LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN BCL 2; RECEPTOR TYPE TYROSINE PROTEIN PHOSPHATASE C; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR; LECTIN; POLYSACCHARIDE;

AUTOIMMUNITY; CELL ACTIVITY; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; HUMAN; IMMUNOLOGICAL TOLERANCE; INFLAMMATORY BOWEL DISEASE; MULTIPLE SCLEROSIS; NEOPLASM; NONHUMAN; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; THYMUS; ULCERATIVE COLITIS; ANIMAL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION;

ANIMALS; HUMANS; IMMUNE TOLERANCE; LECTINS, C-TYPE; LYMPHOCYTE ACTIVATION; NEOPLASMS; POLYSACCHARIDES; SELF TOLERANCE; T-LYMPHOCYTES;

EID: 85057432575     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2018.02754     Document Type: Review

References (136)

1. Di Lella S, Sundblad V, Cerliani JP, Guardia CM, Estrin DA, Vasta GR, et al. When galectins recognize glycans: from biochemistry to physiology and back again. Biochemistry (2011) 50:7842-57. doi: 10.1021/bi201121m
2. Vasta GR, Feng C, González-Montalbán N, Mancini J, Yang L, Abernathy K, et al. Functions of galectins as 'self/non-self'-recognition and effector factors. Pathog Dis. (2017) 75:ftx046. doi: 10.1093/femspd/ftx046
3. Brown GD, Willment JA, Whitehead L. C-type lectins in immunity and homeostasis. Nat Rev Immunol. (2018) 18:374-89. doi: 10.1038/s41577-018-0004-8
4. Macauley MS, Crocker PR, Paulson JC. Siglec-mediated regulation of immune cell function in disease. Nat Rev Immunol. (2014) 14:653-66. doi: 10.1038/nri3737
5. Bochner BS, Zimmermann N. Role of siglecs and related glycan-binding proteins in immune responses and immunoregulation. J Allergy Clin Immunol. (2015) 135:598-608. doi: 10.1016/j.jaci.2014.11.031
6. Varki A, Cummings RD, Esko JD, Stanley P, Hart GW, Aebi M, et al., editors. Essentials of Glycobiology. 3rd ed. New York, NY: Cold Spring Harbor (2015)
7. Johnson JL, Jones MB, Ryan SO, Cobb BA. The regulatory power of glycans and their binding partners in immunity. Trends Immunol. (2013) 34:290-8. doi: 10.1016/j.it.2013.01.006
8. Koch U, Radtke F. Mechanisms of T cell development and transformation. Annu Rev Cell Dev Biol. (2011) 27:539-62. doi: 10.1146/annurev-cellbio-092910-154008
9. Kumar BV, Connors TJ, Farber DL. Human T cell development, localization, and function throughout life. Immunity (2018) 48:202-13. doi: 10.1016/j.immuni.2018.01.007
10. Krueger A, Zietara N, Łyszkiewicz M. T cell development by the numbers. Trends Immunol. (2017) 38:128-39. doi: 10.1016/j.it.2016.10.007
11. Rossi FMV, Corbel SY, Merzaban JS, Carlow DA, Gossens K, Duenas J, et al. Recruitment of adult thymic progenitors is regulated by P-selectin and its ligand PSGL-1. Nat Immunol. (2005) 6:626-34. doi: 10.1038/ni1203
12. Sultana DA, Zhang SL, Todd SP, Bhandoola A. Expression of functional P-selectin glycoprotein ligand 1 on hematopoietic progenitors is developmentally regulated. J Immunol. (2012) 188:4385-93. doi: 10.4049/jimmunol.1101116
13. Shah DK, Zú-iga-Pflücker JC. An overview of the intrathymic intricacies of T cell development. J Immunol. (2014) 192:4017-23. doi: 10.4049/jimmunol.1302259
14. Rampal R, Li ASY, Moloney DJ, Georgiou SA, Luther KB, Nita-Lazar A, et al. Lunatic fringe, manic fringe, and radical fringe recognize similar specificity determinants in O-fucosylated epidermal growth factor-like repeats. J Biol Chem. (2005) 280:42454-63. doi: 10.1074/jbc.M509552200
15. Matsuura A, Ito M, Sakaidani Y, Kondo T, Murakami K, Furukawa K, et al. O-linked N-acetylglucosamine is present on the extracellular domain of notch receptors. J Biol Chem. (2008) 283:35486-95. doi: 10.1074/jbc.M806202200
16. Song Y, Kumar V, Wei HX, Qiu J, Stanley P. Lunatic, manic, and radical fringe each promote T and B cell development. J Immunol. (2016) 196:232-43. doi: 10.4049/jimmunol.1402421
17. Koch U, Lacombe TA, Holland D, Bowman JL, Cohen BL, Egan SE, et al. Subversion of the T/B lineage decision in the thymus by lunatic fringe-mediated inhibition of notch-1. Immunity (2001) 15:225-36. doi: 10.1016/S1074-7613(01)00189-3
18. Visan I, Yuan JS, Tan JB, Cretegny K, Guidos CJ. Regulation of intrathymic T-cell development by lunatic fringe? Notch1 interactions. Immunol Rev. (2006) 209:76-94. doi: 10.1111/j.0105-2896.2006.00360.x
19. Boudil A, Matei IR, Shih HY, Bogdanoski G, Yuan JS, Chang SG, et al. IL-7 coordinates proliferation, differentiation and Tcra recombination during thymocyte β-selection. Nat Immunol. (2015) 16:397-405. doi: 10.1038/ni.3122
20. Visan I, Yuan JS, Liu Y, Stanley P, Guidos CJ. Lunatic Fringe enhances competition for Delta-like Notch ligands but does not overcome defective pre-TCR signaling during thymocyte β-selection in vivo. J Immunol. (2010) 185:4609-17. doi: 10.4049/jimmunol.1002008
21. Hart GW, Housley MP, Slawson C. Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature (2007) 446:1017-22. doi: 10.1038/nature05815
22. Hart GW. Minireview series on the thirtieth anniversary of research on O-GlcNAcylation of nuclear and cytoplasmic proteins: nutrient regulation of cellular metabolism and physiology by O-GlcNAcylation. J Biol Chem. (2014) 289:34422-3. doi: 10.1074/jbc.R114.609776
23. Swamy M, Pathak S, Grzes KM, Damerow S, Sinclair L V, van Aalten DMF, et al. Glucose and glutamine fuel protein O-GlcNAcylation to control T cell self-renewal and malignancy. Nat Immunol. (2016) 17:712-20. doi: 10.1038/ni.3439
24. Chou TY, Hart GW, Dang CV. c-Myc is glycosylated at threonine 58, a known phosphorylation site and a mutational hot spot in lymphomas. J Biol Chem. (1995) 270:18961-5. doi: 10.1074/jbc.270.32.18961
25. Marino JH, Tan C, Davis B, Han ES, Hickey M, Naukam R, et al. Disruption of thymopoiesis in ST6Gal I-deficient mice. Glycobiology (2008) 18:719-26. doi: 10.1093/glycob/cwn051
26. Bi S, Baum LG. Sialic acids in T cell development and function. Biochim Biophys Acta (2009) 1790:1599-610. doi: 10.1016/j.bbagen.2009.07.027
27. Moody AM, Chui D, Reche PA, Priatel JJ, Marth JD, Reinherz EL. Developmentally regulated glycosylation of the CD8αβ coreceptor stalk modulates ligand binding. Cell (2001) 107:501-12. doi: 10.1016/S0092-8674(01)00577-3
28. Shih HY, Hao B, Krangel MS. Orchestrating T-cell receptor α gene assembly through changes in chromatin structure and organization. Immunol Res. (2011) 49:192-201. doi: 10.1007/s12026-010-8181-y
29. Takaba H, Takayanagi H. The mechanisms of T cell selection in the thymus. Trends Immunol. (2017) 38:805-16. doi: 10.1016/j.it.2017.07.010
30. Demetriou M, Granovsky M, Quaggin S, Dennis JW. Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature (2001) 409:733-9. doi: 10.1038/35055582
31. Rudd PM, Wormald MR, Stanfield RL, Huang M, Mattsson N, Speir JA, et al. Roles for glycosylation of cell surface receptors involved in cellular immune recognition. J Mol Biol. (1999) 293:351-66. doi: 10.1006/jmbi.1999.3104
32. Kuball J, Hauptrock B, Malina V, Antunes E, Voss RH, Wolfl M, et al. Increasing functional avidity of TCR-redirected T cells by removing defined N-glycosylation sites in the TCR constant domain. J Exp Med. (2009) 206:463-75. doi: 10.1084/jem.20082487
33. Daniels MA, Devine L, Miller JD, Moser JM, Lukacher AE, Altman JD, et al. CD8 binding to MHC class I molecules is influenced by T cell maturation and glycosylation. Immunity (2001) 15:1051-61. doi: 10.1016/S1074-7613(01)00252-7
34. Zhou RW, Mkhikian H, Grigorian A, Hong A, Chen D, Arakelyan A, et al. N-glycosylation bidirectionally extends the boundaries of thymocyte positive selection by decoupling Lck from Ca2+ signaling. Nat Immunol. (2014) 15:1038-45. doi: 10.1038/ni.3007
35. Artyomov MN, Lis M, Devadas S, Davis MM, Chakraborty AK. CD4 and CD8 binding to MHC molecules primarily acts to enhance Lck delivery. Proc Natl Acad Sci USA. (2010) 107:16916-21. doi: 10.1073/pnas.1010568107
36. Clark MC, Baum LG. T cells modulate glycans on CD43 and CD45 during development and activation, signal regulation, and survival. Ann N Y Acad Sci. (2012) 1253:58-67. doi: 10.1111/j.1749-6632.2011.06304.x
37. Marth JD, Grewal PK. Mammalian glycosylation in immunity. Nat Rev Immunol. (2008) 8:874-87. doi: 10.1038/nri2417
38. Rossy J, Williamson DJ, Benzing C, Gaus K. The integration of signaling and the spatial organization of the T cell synapse. Front Immunol. (2012) 3:352. doi: 10.3389/fimmu.2012.00352
39. Barbosa JA, Santos-Aguado J, Mentzer SJ, Strominger JL, Burakoff SJ, Biro PA. Site-directed mutagenesis of class I HLA genes. Role of glycosylation in surface expression and functional recognition. J Exp Med. (1987) 166:1329-50. doi: 10.1084/jem.166.5.1329
40. Unanue ER, Turk V, Neefjes J. Variations in MHC Class II antigen processing and presentation in health and disease. Annu Rev Immunol. (2016) 34:265-97. doi: 10.1146/annurev-immunol-041015-055420
41. Ryan SO, Bonomo JA, Zhao F, Cobb BA. MHCII glycosylation modulates Bacteroides fragilis carbohydrate antigen presentation. J Exp Med. (2011) 208:1041-53. doi: 10.1084/jem.20100508
42. Dias AM, Pereira MS, Padrão NA, Alves I, Marcos-Pinto R, Lago P, et al. Glycans as critical regulators of gut immunity in homeostasis and disease. Cell Immunol. (2018). doi: 10.1016/j.cellimm.2018.07.007. [Epub ahead of print].
43. Fujii H, Shinzaki S, Iijima H, Wakamatsu K, Iwamoto C, Sobajima T, et al. Core Fucosylation on T cells, required for activation of T-cell receptor signaling and induction of colitis in mice, is increased in patients with inflammatory bowel disease. Gastroenterology (2016) 150:1620-32. doi: 10.1053/j.gastro.2016.03.002
44. Wolfert MA, Boons GJ. Adaptive immune activation: glycosylation does matter. Nat Chem Biol. (2013) 9:776-84. doi: 10.1038/nchembio.1403
45. Hermiston ML, Xu Z, Weiss A. CD45: a critical regulator of signaling thresholds in immune cells. Annu Rev Immunol. (2003) 21:107-37. doi: 10.1146/annurev.immunol.21.120601.140946
46. Ohta T, Kitamura K, Maizel AL, Takeda A. Alterations in CD45 glycosylation pattern accompanying different cell proliferation states. Biochem Biophys Res Commun. (1994) 200:1283-9. doi: 10.1006/bbrc.1994.1590
47. Rogers PR, Pilapil S, Hayakawa K, Romain PL, Parker DC. CD45 alternative exon expression in murine and human CD4+ T cell subsets. J Immunol. (1992) 148:4054-65.
48. Furukawa K, Funakoshi Y, Autero M, Horejsi V, Kobata A, Gahmberg CG. Structural study of the O-linked sugar chains of human leukocyte tyrosine phosphatase CD45. Eur J Biochem. (1998) 251:288-94. doi: 10.1046/j.1432-1327.1998.2510288.x
49. Zapata JM, Pulido R, Acevedo A, Sanchez-Madrid F, de Landazuri MO. Human CD45RC specificity. A novel marker for T cells at different maturation and activation stages. J Immunol. (1994) 152:3852-61.
50. Daniels MA, Hogquist KA, Jameson SC. Sweet "n" sour: the impact of differential glycosylation on T cell responses. Nat Immunol. (2002) 3:903-10. doi: 10.1038/ni1002-903
51. Garcia GG, Berger SB, Sadighi Akha AA, Miller RA. Age-associated changes in glycosylation of CD43 and CD45 on mouse CD4 T cells. Eur J Immunol. (2005) 35:622-31. doi: 10.1002/eji.200425538
52. Aruffo A, Seed B. Molecular cloning of a CD28 cDNA by a high-efficiency COS cell expression system. Proc Natl Acad Sci USA. (1987) 84:8573-7. doi: 10.1073/pnas.84.23.8573
53. Araujo L, Khim P, Mkhikian H, Mortales CL, Demetriou M. Glycolysis and glutaminolysis cooperatively control T cell function by limiting metabolite supply to N-glycosylation. Elife (2017) 6:1-16. doi: 10.7554/eLife.21330
54. Chen L, Ashe S, Brady WA, Hellstrom I, Hellstrom KE, Ledbetter JA, et al. Costimulation of antitumor immunity by the B7 counterreceptor for the T lymphocyte molecules CD28 and CTLA-4. Cell (1992) 71:1093-102. doi: 10.1016/S0092-8674(05)80059-5
55. Alegre ML, Frauwirth KA, Thompson CB. T-cell regulation by CD28 and CTLA-4. Nat Rev Immunol. (2001) 1:220-8. doi: 10.1038/35105024
56. Zhu L, Guo Q, Guo H, Liu T, Zheng Y, Gu P, et al. Versatile characterization of glycosylation modification in CTLA4-Ig fusion proteins by liquid chromatography-mass spectrometry. MAbs (2014) 6:1474-85. doi: 10.4161/mabs.36313
57. Monney L, Sabatos CA, Gaglia JL, Ryu A, Waldner H, Chernova T, et al. Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature (2002) 415:536-41. doi: 10.1038/415536a
58. Maverakis E, Kim K, Shimoda M, Gershwin ME, Patel F, Wilken R, et al. Glycans in the immune system and the altered glycan theory of autoimmunity: a critical review. J Autoimmun. (2015) 57:1-13. doi: 10.1016/j.jaut.2014.12.002
59. Lee SU, Grigorian A, Pawling J, Chen IJ, Gao G, Mozaffar T, et al. N-glycan processing deficiency promotes spontaneous inflammatory demyelination and neurodegeneration. J Biol Chem. (2007) 282:33725-34. doi: 10.1074/jbc.M704839200
60. Dias AM, Correia A, Pereira MS, Almeida CR, Alves I, Pinto V, et al. Metabolic control of T cell immune response through glycans in inflammatory bowel disease. Proc Natl Acad Sci USA. (2018) 115:E4651-60. doi: 10.1073/pnas.1720409115
61. Togayachi A, Kozono Y, Ishida H, Abe S, Suzuki N, Tsunoda Y, et al. Polylactosamine on glycoproteins influences basal levels of lymphocyte and macrophage activation. Proc Natl Acad Sci USA. (2007) 104:15829-34. doi: 10.1073/pnas.0707426104
62. Mkhikian H, Mortales CL, Zhou RW, Khachikyan K, Wu G, Haslam SM, et al. Golgi self-correction generates bioequivalent glycans to preserve cellular homeostasis. Elife (2016) 5:e14814. doi: 10.7554/eLife.14814
63. Chui D, Sellakumar G, Green R, Sutton-Smith M, McQuistan T, Marek K, et al. Genetic remodeling of protein glycosylation in vivo induces autoimmune disease. Proc Natl Acad Sci USA. (2001):1142-7. doi: 10.1073/pnas.98.3.1142
64. Green RS, Stone EL, Tenno M, Lehtonen E, Farquhar MG, Marth JD. Mammalian N-glycan branching protects against innate immune self-recognition and inflammation in autoimmune disease pathogenesis. Immunity (2007) 27:308-20. doi: 10.1016/j.immuni.2007.06.008
65. Hashii N, Kawasaki N, Itoh S, Nakajima Y, Kawanishi T, Yamaguchi T. Alteration of N-glycosylation in the kidney in a mouse model of systemic lupus erythematosus: relative quantification of N-glycans using an isotope-tagging method. Immunology (2009) 126:336-45. doi: 10.1111/j.1365-2567.2008.02898.x
66. Ye Z, Marth JD. N-glycan branching requirement in neuronal and postnatal viability. Glycobiology (2004) 14:547-58. doi: 10.1093/glycob/cwh069
67. Darrah E, Andrade F. NETs: the missing link between cell death and systemic autoimmune diseases? Front Immunol. (2013) 3:428. doi: 10.3389/fimmu.2012.00428
68. Miller FW, Lamb JA, Schmidt J, Nagaraju K. Risk factors and disease mechanisms in myositis. Nat Rev Rheumatol. (2018) 14:255-68. doi: 10.1038/nrrheum.2018.48
69. McMorran BJ, McCarthy FE, Gibbs EM, Pang M, Marshall JL, Nairn A V, et al. Differentiation-related glycan epitopes identify discrete domains of the muscle glycocalyx. Glycobiology (2016) 26:1120-32. doi: 10.1093/glycob/cww061
70. Townsend D. Finding the sweet spot: assembly and glycosylation of the dystrophin-associated glycoprotein complex. Anat Rec. (2014) 297:1694-705. doi: 10.1002/ar.22974
71. Malicdan MCV, Noguchi S, Hayashi YK, Nonaka I, Nishino I. Prophylactic treatment with sialic acid metabolites precludes the development of the myopathic phenotype in the DMRV-hIBM mouse model. Nat Med. (2009) 15:690-5. doi: 10.1038/nm.1956
72. Szabó TG, Palotai R, Antal P, Tokatly I, Tóthfalusi L, Lund O, et al. Critical role of glycosylation in determining the length and structure of T cell epitopes. Immunome Res. (2009) 5:4. doi: 10.1186/1745-7580-5-4
73. van Kooyk Y, Rabinovich GA. Protein-glycan interactions in the control of innate and adaptive immune responses. Nat Immunol. (2008) 9:593-601. doi: 10.1038/ni.f.203
74. Diana J, Moura IC, Vaugier C, Gestin A, Tissandie E, Beaudoin L, et al. Secretory IgA induces tolerogenic dendritic cells through SIGNR1 dampening autoimmunity in mice. J Immunol. (2013) 191:2335-43. doi: 10.4049/jimmunol.1300864
75. Ilarregui JM, Croci DO, Bianco GA, Toscano MA, Salatino M, Vermeulen ME, et al. Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat Immunol. (2009) 10:981-91. doi: 10.1038/ni.1772
76. Toscano MA, Bianco GA, Ilarregui JM, Croci DO, Correale J, Hernandez JD, et al. Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat Immunol. (2007) 8:825-34. doi: 10.1038/ni1482
77. Clemente T, Vieira NJ, Cerliani JP, Adrain C, Luthi A, Dominguez MR, et al. Proteomic and functional analysis identifies galectin-1 as a novel regulatory component of the cytotoxic granule machinery. Cell Death Dis. (2017) 8:e3176. doi: 10.1038/cddis.2017.506
78. Orlacchio A, Sarchielli P, Gallai V, Datti A, Saccardi C, Palmerini CA. Activity levels of a beta1, 6 N-acetylglucosaminyltransferase in lymphomonocytes from multiple sclerosis patients. J Neurol Sci. (1997) 151:177-83. doi: 10.1016/S0022-510X(97)00117-2
79. Brynedal B, Wojcik J, Esposito F, Debailleul V, Yaouanq J, Martinelli-Boneschi F, et al. MGAT5 alters the severity of multiple sclerosis. J Neuroimmunol. (2010) 220:120-4. doi: 10.1016/j.jneuroim.2010.01.003
80. Mkhikian H, Grigorian A, Li CF, Chen HL, Newton B, Zhou RW, et al. Genetics and the environment converge to dysregulate N-glycosylation in multiple sclerosis. Nat Commun. (2011) 2:334. doi: 10.1038/ncomms1333
81. Grigorian A, Mkhikian H, Li CF, Newton BL, Zhou RW, Demetriou M. Pathogenesis of multiple sclerosis via environmental and genetic dysregulation of N-glycosylation. Semin Immunopathol. (2012) 34:415-24. doi: 10.1007/s00281-012-0307-y
82. Li CF, Zhou RW, Mkhikian H, Newton BL, Yu Z, Demetriou M. Hypomorphic MGAT5 polymorphisms promote multiple sclerosis cooperatively with MGAT1 and interleukin-2 and 7 receptor variants. J Neuroimmunol. (2013) 256:71-6. doi: 10.1016/j.jneuroim.2012.12.008
83. Dias AM, Dourado J, Lago P, Cabral J, Marcos-Pinto R, Salgueiro P, et al. Dysregulation of T cell receptor N-glycosylation: a molecular mechanism involved in ulcerative colitis. Hum Mol Genet. (2014) 23:2416-27. doi: 10.1093/hmg/ddt632
84. Pereira MS, Maia L, Azevedo LF, Campos S, Carvalho S, Dias AM, et al. A [Glyco]biomarker that predicts failure to standard therapy in ulcerative colitis patients. J Crohns Colitis (2018). doi: 10.1093/ecco-jcc/jjy139. [Epub ahead of print].
85. Grigorian A, Araujo L, Naidu NN, Place DJ, Choudhury B, Demetriou M. N -Acetylglucosamine Inhibits T-helper 1 (Th1)/T-helper 17 (Th17) cell responses and treats experimental autoimmune encephalomyelitis. J Biol Chem. (2011) 286:40133-41. doi: 10.1074/jbc.M111.277814
86. McMorran BJ, Miceli MC, Baum LG. Lectin-binding characterizes the healthy human skeletal muscle glycophenotype and identifies disease-specific changes in dystrophic muscle. Glycobiology (2017) 27:1134-43. doi: 10.1093/glycob/cwx073
87. Balasubramanian M, Johnson DS, DDD Study. MAN1B-CDG: Novel variants with a distinct phenotype and review of literature. Eur J Med Genet. (2018). doi: 10.1016/j.ejmg.2018.06.011. [Epub ahead of print].
88. Wiendl H, Hohlfeld R, Kieseier BC. Immunobiology of muscle: advances in understanding an immunological microenvironment. Trends Immunol. (2005) 26:373-80. doi: 10.1016/j.it.2005.05.003
89. Afzali AM, Müntefering T, Wiendl H, Meuth SG, Ruck T. Skeletal muscle cells actively shape (auto)immune responses. Autoimmun Rev. (2018) 17:518-29. doi: 10.1016/j.autrev.2017.12.005
90. RodrÍguez E, Schetters STT, van Kooyk Y. The tumour glyco-code as a novel immune checkpoint for immunotherapy. Nat Rev Immunol. (2018) 18:204-11. doi: 10.1038/nri.2018.3
91. Blank C, Mackensen A. Contribution of the PD-L1/PD-1 pathway to T-cell exhaustion: an update on implications for chronic infections and tumor evasion. Cancer Immunol Immunother. (2007) 56:739-45. doi: 10.1007/s00262-006-0272-1
92. Okada M, Chikuma S, Kondo T, Hibino S, Machiyama H, Yokosuka T, et al. Blockage of core Fucosylation reduces cell-surface expression of PD-1 and promotes anti-tumor immune responses of T cells. Cell Rep. (2017) 20:1017-28. doi: 10.1016/j.celrep.2017.07.027
93. Li CW, Lim SO, Xia W, Lee HH, Chan LC, Kuo CW, et al. Glycosylation and stabilization of programmed death ligand-1 suppresses T-cell activity. Nat Commun. (2016) 7:12632. doi: 10.1038/ncomms12632
94. Li CW, Lim SO, Chung EM, Kim YS, Park AH, Yao J, et al. Eradication of triple-negative breast cancer cells by targeting Glycosylated PD-L1. Cancer Cell. (2018) 33:187-201.e10. doi: 10.1016/j.ccell.2018.01.009
95. Cabral J, Hanley SA, Gerlach JQ, O'Leary N, Cunningham S, Ritter T, et al. Distinctive surface Glycosylation patterns associated with mouse and human CD4+ regulatory T cells and their suppressive function. Front Immunol. (2017) 8:987. doi: 10.3389/fimmu.2017.00987
96. Dennis JW, Lau KS, Demetriou M, Nabi IR. Adaptive regulation at the cell surface by N-glycosylation. Traffic (2009) 10:1569-78. doi: 10.1111/j.1600-0854.2009.00981.x
97. Pinho SS, Reis CA. Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer (2015) 15:540-55. doi: 10.1038/nrc3982
98. Rodrigues JG, Balmaña M, Macedo JA, Poças J, Fernandes Â, De-Freitas-Junior JCM, et al. Glycosylation in cancer: selected roles in tumour progression, immune modulation and metastasis. Cell Immunol. (2018). doi: 10.1016/j.cellimm.2018.03.007. [Epub ahead of print].
99. van Liempt E, Bank CMC, Mehta P, Garci'a-Vallejo JJ, Kawar ZS, Geyer R, et al. Specificity of DC-SIGN for mannose- and fucose-containing glycans. FEBS Lett. (2006) 580:6123-31. doi: 10.1016/j.febslet.2006.10.009
100. van Gisbergen KPJM, Aarnoudse CA, Meijer GA, Geijtenbeek TBH, van Kooyk Y. Dendritic cells recognize tumor-specific glycosylation of carcinoembryonic antigen on colorectal cancer cells through dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin. Cancer Res. (2005) 65:5935-44. doi: 10.1158/0008-5472.CAN-04-4140
101. Gringhuis SI, Kaptein TM, Wevers BA, van der Vlist M, Klaver EJ, van Die I, et al. Fucose-based PAMPs prime dendritic cells for follicular T helper cell polarization via DC-SIGN-dependent IL-27 production. Nat Commun. (2014) 5:5074. doi: 10.1038/ncomms6074
102. García-Vallejo JJ, Ilarregui JM, Kalay H, Chamorro S, Koning N, Unger WW, et al. CNS myelin induces regulatory functions of DC-SIGN-expressing, antigen-presenting cells via cognate interaction with MOG. J Exp Med. (2014) 211:1465-83. doi: 10.1084/jem.20122192
103. Unger WWJ, van Beelen AJ, Bruijns SC, Joshi M, Fehres CM, van Bloois L, et al. Glycan-modified liposomes boost CD4+ and CD8+ T-cell responses by targeting DC-SIGN on dendritic cells. J Control Release (2012) 160:88-95. doi: 10.1016/j.jconrel.2012.02.007
104. van Vliet SJ, Bay S, Vuist IM, Kalay H, García-Vallejo JJ, Leclerc C, et al. MGL signaling augments TLR2-mediated responses for enhanced IL-10 and TNF-α secretion. J Leukoc Biol. (2013) 94:315-23. doi: 10.1189/jlb.1012520
105. van Vliet SJ, Gringhuis SI, Geijtenbeek TBH, van Kooyk Y. Regulation of effector T cells by antigen-presenting cells via interaction of the C-type lectin MGL with CD45. Nat Immunol. (2006) 7:1200-8. doi: 10.1038/ni1390
106. Ruffell B, Chang-Strachan D, Chan V, Rosenbusch A, Ho CMT, Pryer N, et al. Macrophage IL-10 blocks CD8+ T cell-dependent responses to chemotherapy by suppressing IL-12 expression in intratumoral dendritic cells. Cancer Cell (2014) 26:623-37. doi: 10.1016/j.ccell.2014.09.006
107. Smith LK, Boukhaled GM, Condotta SA, Mazouz S, Guthmiller JJ, Vijay R, et al. Interleukin-10 directly inhibits CD8(+) T cell function by enhancing N-Glycan branching to decrease antigen sensitivity. Immunity (2018) 48:299-312 e5. doi: 10.1016/j.immuni.2018.01.006
108. Perdicchio M, Ilarregui JM, Verstege MI, Cornelissen LAM, Schetters STT, Engels S, et al. Sialic acid-modified antigens impose tolerance via inhibition of T-cell proliferation and de novo induction of regulatory T cells. Proc Natl Acad Sci USA. (2016) 113:3329-34. doi: 10.1073/pnas.1507706113
109. Perdicchio M, Cornelissen LAM, Streng-Ouwehand I, Engels S, Verstege MI, Boon L, et al. Tumor sialylation impedes T cell mediated anti-tumor responses while promoting tumor associated-regulatory T cells. Oncotarget (2016) 7:8771-82. doi: 10.18632/oncotarget.6822
110. Beatson R, Tajadura-Ortega V, Achkova D, Picco G, Tsourouktsoglou TD, Klausing S, et al. The mucin MUC1 modulates the tumor immunological microenvironment through engagement of the lectin Siglec-9. Nat Immunol. (2016) 17:1273-81. doi: 10.1038/ni.3552
111. Carrascal MA, Severino PF, Guadalupe Cabral M, Silva M, Ferreira JA, Calais F, et al. Sialyl Tn-expressing bladder cancer cells induce a tolerogenic phenotype in innate and adaptive immune cells. Mol Oncol. (2014) 8:753-65. doi: 10.1016/j.molonc.2014.02.008
112. Julien S, Videira PA, Delannoy P. Sialyl-tn in cancer: (how) did we miss the target? Biomolecules (2012):435-66. doi: 10.3390/biom2040435
113. Stanczak MA, Siddiqui SS, Trefny MP, Thommen DS, Boligan KF, von Gunten S, et al. Self-associated molecular patterns mediate cancer immune evasion by engaging Siglecs on T cells. J Clin Invest. (2018) 128:4912-23. doi: 10.1172/JCI120612
114. Garín MI, Chu C-C, Golshayan D, Cernuda-Morollón E, Wait R, Lechler RI. Galectin-1: a key effector of regulation mediated by CD4+CD25+ T cells. Blood (2007) 109:2058-65. doi: 10.1182/blood-2006-04-016451
115. Stillman BN, Hsu DK, Pang M, Brewer CF, Johnson P, Liu F-T, et al. Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J Immunol. (2006) 176:778-89. doi: 10.4049/jimmunol.176.2.778
116. Matarrese P, Tinari A, Mormone E, Bianco GA, Toscano MA, Ascione B, et al. Galectin-1 sensitizes resting human T lymphocytes to Fas (CD95)-mediated cell death via mitochondrial hyperpolarization, budding, and fission. J Biol Chem. (2005) 280:6969-85. doi: 10.1074/jbc.M409752200
117. Rabinovich GA, van Kooyk Y, Cobb BA. Glycobiology of immune responses. Ann N Y Acad Sci. (2012) 1253:1-15. doi: 10.1111/j.1749-6632.2012.06492.x
118. Yang RY, Hsu DK, Liu FT. Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Natl Acad Sci USA. (1996) 93:6737-42. doi: 10.1073/pnas.93.13.6737
119. Lau KS, Partridge EA, Grigorian A, Silvescu CI, Reinhold VN, Demetriou M, et al. Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell (2007) 129:123-34. doi: 10.1016/j.cell.2007.01.049
120. Kouo T, Huang L, Pucsek AB, Cao M, Solt S, Armstrong T, et al. Galectin-3 shapes antitumor immune responses by suppressing CD8+ T cells via LAG-3 and inhibiting expansion of Plasmacytoid dendritic cells. Cancer Immunol Res. (2015) 3:412-23. doi: 10.1158/2326-6066.CIR-14-0150
121. Zhu C, Anderson AC, Schubart A, Xiong H, Imitola J, Khoury SJ, et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol. (2005) 6:1245-52. doi: 10.1038/ni1271
122. Oomizu S, Arikawa T, Niki T, Kadowaki T, Ueno M, Nishi N, et al. Galectin-9 suppresses Th17 cell development in an IL-2-dependent but Tim-3-independent manner. Clin Immunol. (2012) 143:51-8. doi: 10.1016/j.clim.2012.01.004
123. Kang CW, Dutta A, Chang LY, Mahalingam J, Lin YC, Chiang JM, et al. Apoptosis of tumor infiltrating effector TIM-3+CD8+ T cells in colon cancer. Sci Rep. (2015) 5:15659. doi: 10.1038/srep15659
124. Su EW, Bi S, Kane LP. Galectin-9 regulates T helper cell function independently of Tim-3. Glycobiology (2011) 21:1258-65. doi: 10.1093/glycob/cwq214
125. Almeida L, Lochner M, Berod L, Sparwasser T. Metabolic pathways in T cell activation and lineage differentiation. Semin Immunol. (2016) 28:514-24. doi: 10.1016/j.smim.2016.10.009
126. Wang T, Marquardt C, Foker J. Aerobic glycolysis during lymphocyte proliferation. Nature (1976) 261:702-5. doi: 10.1038/261702a0
127. Wang R, Green DR. Metabolic checkpoints in activated T cells. Nat Immunol. (2012) 13:907-15. doi: 10.1038/ni.2386
128. Wellen KE, Thompson CB. A two-way street: reciprocal regulation of metabolism and signalling. Nat Rev Mol Cell Biol. (2012) 13:270-6. doi: 10.1038/nrm3305
129. Abdel Rahman AM, Ryczko M, Pawling J, Dennis JW. Probing the hexosamine biosynthetic pathway in human tumor cells by multitargeted tandem mass spectrometry. ACS Chem Biol. (2013) 8:2053-62. doi: 10.1021/cb4004173
130. Grigorian A, Lee SU, Tian W, Chen IJ, Gao G, Mendelsohn R, et al. Control of T cell-mediated autoimmunity by metabolite flux to N-glycan biosynthesis. J Biol Chem. (2007) 282:20027-35. doi: 10.1074/jbc.M701890200
131. Love DC, Hanover JA. The hexosamine signaling pathway: deciphering the "O-GlcNAc code". Sci STKE (2005) 2005:re13. doi: 10.1126/stke.3122005re13
132. Kreppel LK, Hart GW. Regulation of a cytosolic and nuclear O-GlcNAc transferase. Role of the tetratricopeptide repeats. J Biol Chem. (1999) 274:32015-22. doi: 10.1074/jbc.274.45.32015
133. Sasai K, Ikeda Y, Fujii T, Tsuda T, Taniguchi N. UDP-GlcNAc concentration is an important factor in the biosynthesis of beta1, 6-branched oligosaccharides: regulation based on the kinetic properties of N-acetylglucosaminyltransferase V. Glycobiology (2002) 12:119-27. doi: 10.1093/glycob/12.2.119
134. Ryczko MC, Pawling J, Chen R, Abdel Rahman AM, Yau K, Copeland JK, et al. Metabolic reprogramming by hexosamine biosynthetic and golgi N-Glycan branching pathways. Sci Rep. (2016) 6:23043. doi: 10.1038/srep23043
135. Chien MW, Lin MH, Huang SH, Fu SH, Hsu CY, Yen BLJ, et al. Glucosamine modulates T cell differentiation through down-regulating N-linked Glycosylation of CD25. J Biol Chem. (2015) 290:29329-44. doi: 10.1074/jbc.M115.674671
136. Zhang GX, Yu S, Gran B, Rostami A. Glucosamine abrogates the acute phase of experimental autoimmune encephalomyelitis by induction of Th2 response. J Immunol. (2005) 175:7202-8. doi: 10.4049/jimmunol.175.11.7202