Acute phase inflammation is characterized by rapid changes in plasma/peritoneal fluid N-glycosylation in mice

Glycoconjugate Journal

Volumn 33, Issue 3, 2016, Pages 457-470

  Rombouts, Yoann ^a,b   Jónasdóttir, Hulda S ^a   Hipgrave Ederveen, Agnes L ^a   Reiding, Karli R ^a   Jansen, Bas C ^a   Freysdottir, Jona ^c,d   Hardardottir, Ingibjörg ^c   Ioan Facsinay, Andreea ^a   Giera, Martin ^a   Wuhrer, Manfred ^a,e  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c UNIVERSITY OF ICELAND   (Iceland)

^d LANDSPITALI UNIVERSITY HOSPITAL   (Iceland)

^e VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Mouse; N glycosylation changes; Peritoneal fluid; Plasma; Zymosan induced peritonitis

Indexed keywords

IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; INTERLEUKIN 6; LEUKOTRIENE B4; N ACETYLGLUCOSAMINE; N GLYCOLOYLNEURAMINIC ACID; SIALIC ACID; ZYMOSAN; GLYCOPROTEIN;

ACUTE PHASE RESPONSE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOHYDRATE ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; DERIVATIZATION; FEMALE; FUCOSYLATION; GALACTOSYLATION; GLYCOSYLATION AND DEGLYCOSYLATION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NONHUMAN; PERITONEAL FLUID; PERITONEUM MACROPHAGE; PLASMA; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SIALYLATION; STRUCTURE ANALYSIS; ZYMOSAN-INDUCED PERITONITIS; ANALOGS AND DERIVATIVES; ANIMAL; ASCITES FLUID; BLOOD; C57BL MOUSE; CHEMISTRY; GLYCOSYLATION; METABOLISM; PERITONITIS; PROTEIN PROCESSING;

ACETYLGLUCOSAMINE; ACUTE-PHASE REACTION; ANIMALS; ASCITIC FLUID; FEMALE; GLYCOPROTEINS; GLYCOSYLATION; MICE; MICE, INBRED C57BL; PERITONITIS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84959340970     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-015-9648-9     Document Type: Article

References (72)

1. Nathan C.: Points of control in inflammation. Nature. 420, 846–852 (2002)
2. Lawrence T., Gilroy D.W.: Chronic inflammation: a failure of resolution? Int. J. Exp. Pathol. 88, 85–94 (2007)
3. Lee C.H.: Resolvins as new fascinating drug candidates for inflammatory diseases. Arch. Pharm. Res. 35, 3–7 (2012)
4. Lawrence T., Willoughby D.A., Gilroy D.W.: Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat. Rev. Immunol. 2, 787–795 (2002)
5. Bannenberg G.L.: Therapeutic applicability of anti-inflammatory and proresolving polyunsaturated fatty acidderived lipid mediators. Sci. World J. 10, 676–712 (2010)
6. Gabay C., Kushner I.: Acute-phase proteins and other systemic responses to inflammation. N. Engl. J. Med. 340, 448–454 (1999)
7. Shanley T.P., Warner R.L., Ward P.A.: The role of cytokines and adhesion molecules in the development of inflammatory injury. Mol. Med. Today. 1, 40–45 (1995)
8. Jenny N.S., Cushman M.: C-reactive protein: initiator or product of inflammation? Circ. Res. 114, 596–597 (2014)
9. Ariel A., Serhan C.N.: New lives given by cell death: macrophage differentiation following their encounter with apoptotic leukocytes during the resolution of inflammation. Front. Immunol. 3, 4 (2012)
10. Seki H., Tani Y., Arita M.: Omega-3 PUFA derived anti-inflammatory lipid mediator resolvin E1. Prostaglandins Other Lipid Mediat. 89, 126–130 (2009)
11. Serhan C.N.: Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu. Rev. Immunol. 25, 101–137 (2007)
12. Dalli J., Serhan C.N.: Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood. 120, e60–e72 (2012)
13. McCarthy C., Saldova R., Wormald M.R., Rudd P.M., McElvaney N.G., Reeves E.P.: The role and importance of glycosylation of acute phase proteins with focus on alpha-1 antitrypsin in acute and chronic inflammatory conditions. J. Proteome Res. 13, 3131–3143 (2014)
14. Barthel S.R., Gavino J.D., Descheny L., Dimitroff C.J.: Targeting selectins and selectin ligands in inflammation and cancer. Expert Opin. Ther. Targets. 11, 1473–1491 (2007)
15. Lowe J.B.: Glycan-dependent leukocyte adhesion and recruitment in inflammation. Curr. Opin. Cell Biol. 15, 531–538 (2003)
16. Zauner G., Selman M.H.J., Bondt A., Rombouts Y., Blank D., Deelder A.M., Wuhrer M.: Glycoproteomic analysis of antibodies. Mol. Cell. Proteomics. 12, 856–865 (2013)
17. Bondt A., Selman M.H.J., Deelder A.M., Hazes J.M.W., Willemsen S.P., Wuhrer M., Dolhain R.J.E.M.: Association between galactosylation of immunoglobulin G and improvement of rheumatoid arthritis during pregnancy is independent of sialylation. J. Proteome Res. 12, 4522–4531 (2013)
18. Novokmet M., Lukić E., Vučković F., Ðurić Ž., Keser T., Rajšl K., Remondini D., Castellani G., Gašparović H., Gornik O., Lauc G.: Changes in IgG and total plasma protein glycomes in acute systemic inflammation. Sci. Rep. 4, 4347 (2014)
19. Collins E.S., Galligan M.C., Saldova R., Adamczyk B., Abrahams J.L., Campbell M.P., Ng C.T., Veale D.J., Murphy T.B., Rudd P.M., Fitzgerald O.: Glycosylation status of serum in inflammatory arthritis in response to anti-TNF treatment. Rheumatology. 52, 1572–1582 (2013)
20. Reiding K.R., Blank D., Kuijper D.M., Deelder A.M., Wuhrer M.: High-throughput profiling of protein Nglycosylation by MALDI-TOF-MS employing linkage-specific sialic acid esterification. Anal. Chem. 86, 5784–5793 (2014)
21. Bladergroen, M.R., Reiding, K.R., Hipgrave-Ederveen, A.L., Vreeker, G.C.M., Clerc, F., Holst, S., Bondt, A., Wuhrer, M. Van der Burgt, Y.E.M.: Automation of high-throughput mass spectrometry-based plasma N-glycome analysis with linkage-specific sialic acid esterification. J. Proteome Res. (2015)
22. Bondt A., Rombouts Y., Selman M.H.J., Hensbergen P.J., Reiding K.R., Hazes J.M.W., Dolhain R.J.E.M., Wuhrer M.: Immunoglobulin G (IgG) Fab glycosylation analysis using a new mass spectrometric high-throughput profiling method reveals pregnancy-associated changes. Mol. Cell. Proteomics. 13, 3029–3039 (2014)
23. Rao T.S., Currie J.L., Shaffer A.F., Isakson P.C.: In vivo characterization of zymosan-induced mouse peritoneal inflammation. J. Pharmacol. Exp. Ther. 269, 917–925 (1994)
24. Doherty N.S., Poubelle P., Borgeat P., Beaver T.H., Westrich G.L., Schrader N.L.: Intraperitoneal injection of zymosan in mice induces pain, inflammation and the synthesis of peptidoleukotrienes and prostaglandin E2. Prostaglandins. 30, 769–789 (1985)
25. Cash J.L., White G.E., Greaves D.R.: Chapter 17. Zymosan-induced peritonitis as a simple experimental system for the study of inflammation. Methods Enzymol. 461, 379–396 (2009)
26. Bannenberg G.L., Chiang N., Ariel A., Arita M., Tjonahen E., Gotlinger K.H., Hong S., Serhan C.N.: Molecular circuits of resolution: formation and actions of resolvins and protectins. J. Immunol. 174, 4345–4355 (2005)
27. Rossi A., Pergola C., Pace S., Rådmark O., Werz O., Sautebin L.: In vivo sex differences in leukotriene biosynthesis in zymosan-induced peritonitis. Pharmacol. Res. 87, 1–7 (2014)
28. Giera M., Ioan-Facsinay A., Toes R., Gao F., Dalli J., Deelder A.M., Serhan C.N., Mayboroda O.A.: Lipid and lipid mediator profiling of human synovial fluid in rheumatoid arthritis patients by means of LC-MS/MS. Biochim. Biophys. Acta. 1821, 1415–1424 (2012)
29. Schlegel M., Köhler D., Körner A., Granja T., Straub A., Giera M., Mirakaj V.: The neuroimmune guidance cue netrin-1 controls resolution programs and promotes liver regeneration. Hepatology. (2015). doi:10.1002/hep.28347
30. Ruhaak L.R., Huhn C., Waterreus W.-J., de Boer A.R., Neusüss C., Hokke C.H., Deelder A.M., Wuhrer M.: Hydrophilic interaction chromatography-based high-throughput sample preparation method for N-glycan analysis from total human plasma glycoproteins. Anal. Chem. 80, 6119–6126 (2008)
31. Selman M.H.J., Hemayatkar M., Deelder A.M., Wuhrer M.: Cotton HILIC SPE microtips for microscale purification and enrichment of glycans and glycopeptides. Anal. Chem. 83, 2492–2499 (2011)
32. GlycoWorkbench, https://code.google.com/p/glycoworkbench/
33. Selman M.H.J., Derks R.J.E., Bondt A., Palmblad M., Schoenmaker B., Koeleman C.A.M., van de Geijn F.E., Dolhain R.J.E.M., Deelder A.M., Wuhrer M.: Fc specific IgG glycosylation profiling by robust Nano-reverse phase HPLC-MS using a sheath-flow ESI sprayer interface. J. Proteome. 75, 1318–1329 (2012)
34. Harre U., Lang S.C., Pfeifle R., Rombouts Y., Frühbeißer S., Amara K., Bang H., Lux A., Koeleman C.A., Baum W., Dietel K., Gröhn F., Malmström V., Klareskog L., Krönke G., Kocijan R., Nimmerjahn F., Toes R.E.M., Herrmann M., Scherer H.-U., Schett G.: Glycosylation of immunoglobulin G determines osteoclast differentiation and bone loss. Nat. Commun. 6, 6651 (2015)
35. Jansen B.C., Reiding K.R., Bondt A., Hipgrave-Ederveen A.L., Palmblad M., Falck D., Wuhrer M.: MassyTools: a high-throughput targeted data processing tool for relative quantitation and quality control developed for glycomic and glycoproteomic MALDI-MS. J. Proteome Res. 14, 5088–5098 (2015)
36. Lin S.-Y., Chen Y.-Y., Fan Y.-Y., Lin C.-W., Chen S.-T., Wang A.H.-J., Khoo K.-H.: Precise mapping of increased sialylation pattern and the expression of acute phase proteins accompanying murine tumor progression in BALB/c mouse by integrated sera proteomics and glycomics. J. Proteome Res. 7, 3293–3303 (2008)
37. Saldova R., Piccard H., Pérez-Garay M., Harvey D.J., Struwe W.B., Galligan M.C., Berghmans N., Madden S.F., Peracaula R., Opdenakker G., Rudd P.M.: Increase in sialylation and branching in the mouse serum Nglycome correlates with inflammation and ovarian tumour progression. PLoS ONE. 8, e71159 (2013)
38. Hua S., Jeong H.N., Dimapasoc L.M., Kang I., Han C., Choi J.-S., Lebrilla C.B., An H.J.: Isomer-specific LC/MS and LC/MS/MS profiling of the mouse serum N-glycome revealing a number of novel sialylated N-glycans. Anal. Chem. 85, 4636–4643 (2013)
39. Coddeville, B., Regoeczi, E., Strecker, G., Plancke, Y.: Structural analysis of trisialylated biantennary glycans isolated from mouse serum transferrin: characterization of the sequence Neu5Gc (α2–3) gal (β1–3)[Neu5Gc α2-et biophysica acta (BBA) (2000)
40. Fujieda Y., Manno A., Hayashi Y., Rhodes N., Guo L., Arita M., Bamba T., Fukusaki E.: Inflammation and resolution are associated with upregulation of fatty acid β-oxidation in zymosan-induced peritonitis. PLoS ONE. 8, e66270 (2013)
41. Davies L.C., Rosas M., Jenkins S.J., Liao C.-T., Scurr M.J., Brombacher F., Fraser D.J., Allen J.E., Jones S.A., Taylor P.R.: Distinct bone marrow-derived and tissue-resident macrophage lineages proliferate at key stages during inflammation. Nat. Commun. 4, 1886 (2013)
42. Varki A., Gagneux P.: Multifarious roles of sialic acids in immunity. Ann. N. Y. Acad. Sci. 1253, 16–36 (2012)
43. Lee A., Chick J.M., Kolarich D., Haynes P.A., Robertson G.R., Tsoli M., Jankova L., Clarke S.J., Packer N.H., Baker M.S.: Liver membrane proteome glycosylation changes in mice bearing an extra-hepatic tumor. Mol. Cell. Proteomics. 10, M900538MCP200 (2011)
44. Harvey D.J.: Structural determination ofN-linked glycans by matrix-assisted laser desorption/ionization and electrospray ionization mass spectrometry. Proteomics. 5, 1774–1786 (2005)
45. Arnold J.N., Wormald M.R., Sim R.B., Rudd P.M., Dwek R.A.: The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 25, 21–50 (2007)
46. Pincetic A., Bournazos S., DiLillo D.J., Maamary J., Wang T.T., Dahan R., Fiebiger B.-M., Ravetch J.V.: Type I and type II Fc receptors regulate innate and adaptive immunity. Nat. Immunol. 15, 707–716 (2014)
47. Anthony R.M., Wermeling F., Karlsson M.C.I., Ravetch J.V.: Identification of a receptor required for the antiinflammatory activity of IVIG. Proc. Natl. Acad. Sci. 105, 19571–19578 (2008)
48. Rombouts Y., Ewing E., Stadt L.A., Selman M.H.J., Trouw L.A., Deelder A.M., Huizinga T.W.J., Wuhrer M., Schaardenburg D.V., Toes R.E.M., Scherer H.U.: Anti-citrullinated protein antibodies acquire a pro-inflammatory Fc glycosylation phenotype prior to the onset of rheumatoid arthritis. Ann. Rheum. Dis. 74, 234–241 (2015)
49. Scherer H.U., van der Woude D., Ioan-Facsinay A., el Bannoudi H., Trouw L.A., Wang J., Häupl T., Burmester G.-R., Deelder A.M., Huizinga T.W.J., Wuhrer M., Toes R.E.M.: Glycan profiling of anti-citrullinated protein antibodies isolated from human serum and synovial fluid. Arthritis Rheum. 62, 1620–1629 (2010)
50. Medzihradszky K.F., Kaasik K., Chalkley R.J.: Tissue-specific glycosylation at the glycopeptide level. Mol. Cell. Proteomics. 14, 2103–2110 (2015)
51. Havenaar E.C., Hoff R.C., van den Eijnden D.H., van Dijk W.: Sialyl Lewis(x) epitopes do not occur on acute phase proteins in mice: relationship to the absence of alpha3-fucosyltransferase in the liver. Glycoconj. J. 15, 389–395 (1998)
52. Brinkman-van der Linden E.C., de Haan P.F., Havenaar E.C., van Dijk W.: Inflammation-induced expression of sialyl LewisX is not restricted to alpha1-acid glycoprotein but also occurs to a lesser extent on alpha1-antichymotrypsin and haptoglobin. Glycoconj. J. 15, 177–182 (1998)
53. Brinkman-van der Linden E.C., Van Ommen E.C., van Dijk W.: Glycosylation of alpha 1-acid glycoprotein in septic shock: changes in degree of branching and in expression of sialyl Lewis(x) groups. Glycoconj. J. 13, 27–31 (1996)
54. van Dijk W., Brinkman-van der Linden E.C., Havenaar E.C.: Occurrence and possible function of inflammationinduced expression of sialyl Lewis-x on acute-phase proteins. Adv. Exp. Med. Biol. 435, 145–150 (1998)
55. Gornik O., Royle L., Harvey D.J., Radcliffe C.M., Saldova R., Dwek R.A., Rudd P., Lauc G.: Changes of serum glycans during sepsis and acute pancreatitis. Glycobiology. 17, 1321–1332 (2007)
56. Arnold J.N., Saldova R., Hamid U.M.A., Rudd P.M.: Evaluation of the serum N-linked glycome for the diagnosis of cancer and chronic inflammation. Proteomics. 8, 3284–3293 (2008)
57. Gornik O., Gornik I., Gašparović V., Lauc G.: Change in transferrin sialylation is a potential prognostic marker for severity of acute pancreatitis. Clin. Biochem. 41, 504–510 (2008)
58. Gornik O., Gornik I., Kolednjak I.Z., Lauc G.: Change of transferrin sialylation differs between mild sepsis and severe sepsis and septic shock. Intern. Med. 50, 861–869 (2011)
59. Yasukawa Z., Sato C., Kitajima K.: Inflammation-dependent changes in alpha2,3-, alpha2,6-, and alpha2,8-sialic acid glycotopes on serum glycoproteins in mice. Glycobiology. 15, 827–837 (2005)
60. Chavan M.M., Kawle P.D., Mehta N.G.: Increased sialylation and defucosylation of plasma proteins are early events in the acute phase response. Glycobiology. 15, 838–848 (2005)
61. Paulson J.C., Weinstein J., de Souza-e-Silva U.: Biosynthesis of a disialylated sequence in N-linked oligosaccharides: identification of an N-acetylglucosaminide (alpha 2—-6)-sialyltransferase in Golgi apparatus from rat liver. Eur. J. Biochem. 140, 523–530 (1984)
62. de Heij H.T., Koppen P.L., van den Eijnden D.H.: Biosynthesis of disialylated beta-D-galactopyranosyl-(1—-3)-2-acetamido-2-deoxy-beta-D-glucopy ran osyl oligosaccharide chains. Identification of a beta-D-galactoside alpha-(2—-3)- and a 2-acetamido-2-deoxy-beta-D-glucoside alpha-(2—-6)-sialyltransferase in regenerating rat liver and other tissues. Carbohydr. Res. 149, 85–99 (1986)
63. S. T.: Characterization of mouse sialyltransferase genes: their evolution and diversity. Biosci. Biotechnol. Biochem. 72, 1155–1167 (2008)
64. Gomez C.R., Goral J., Ramirez L., Kopf M., Kovacs E.J.: Aberrant acute-phase response in aged interleukin-6 knockout mice. Shock. 25, 581–585 (2006)
65. Cray C., Zaias J., Altman N.H.: Acute phase response in animals: a review. Comp. Med. 59, 517–526 (2009)
66. Wait R., Chiesa G., Parolini C., Miller I., Begum S., Brambilla D., Galluccio L., Ballerio R., Eberini I., Gianazza E.: Reference maps of mouse serum acute-phase proteins: changes with LPS-induced inflammation and apolipoprotein a-I and a-II transgenes. Proteomics. 5, 4245–4253 (2005)
67. van Dijk W., Mackiewicz A.: Interleukin-6-type cytokine-induced changes in acute phase protein glycosylation. Ann. N. Y. Acad. Sci. 762, 319–330 (1995)
68. Gornik O., Lauc G.: Glycosylation of serum proteins in inflammatory diseases. Dis. Markers. 25, 267–278 (2008)
69. Horowitz, M.: The glycoconjugates V4. Elsevier (2012)
70. Jones M.B., Nasirikenari M., Lugade A.A., Thanavala Y., Lau J.T.Y.: Anti-inflammatory IgG production requires functional P1 promoter in β-galactoside α2,6-sialyltransferase 1 (ST6Gal-1) gene. J. Biol. Chem. 287, 15365–15370 (2012)
71. Jones M.B., Nasirikenari M., Feng L., Migliore M.T., Choi K.-S., Kazim L., Lau J.T.Y.: Role for hepatic and circulatory ST6Gal-1 sialyltransferase in regulating myelopoiesis. J. Biol. Chem. 285, 25009–25017 (2010)
72. Lee M.M., Nasirikenari M., Manhardt C.T., Ashline D.J., Hanneman A.J., Reinhold V.N., Lau J.T.Y.: Platelets support extracellular sialylation by supplying the sugar donor substrate. J. Biol. Chem. 289, 8742–8748 (2014)