Folia Parasitologica, vol. 62 (2015)

Folia Parasitologica 62:049 (2015) | 10.14411/fp.2015.049

Increased sialylation as a phenomenon in accommodation of the parasitic nematode Trichinella spiralis (Owen, 1835) in skeletal muscle fibres

Rositsa Milcheva1,2, Dimitar Ivanov1, Ivan Iliev1, Russy Russev1, Svetlozara Petkova1, Pavel Babál2
1 Institute of Experimental Morphology, Pathology and Anthropology with Museum, Bulgarian Academy of Sciences, Sofia, Bulgaria;
2 Department of Pathology, Faculty of Medicine, Comenius University in Bratislava, Bratislava, Slovakia

The biology of sialic acids has been an object of interest in many models of acquired and inherited skeletal muscle pathology. The present study focuses on the sialylation changes in mouse skeletal muscle after invasion by the parasitic nematode Trichinella spiralis (Owen, 1835). Asynchronous infection with T. spiralis was induced in mice that were sacrificed at different time points of the muscle phase of the disease. The amounts of free sialic acid, sialylated glycoproteins and total sialyltransferase activity were quantified. Histochemistry with lectins specific for sialic acid was performed in order to localise distribution of sialylated glycoconjugates and to clarify the type of linkage of the sialic acid residues on the carbohydrate chains. Elevated intracellular accumulation of α-2,3- and α-2,6-sialylated glycoconjugates was found only within the affected sarcoplasm of muscle fibres invaded by the parasite. The levels of free and protein-bound sialic acid were increased and the total sialyltransferase activity was also elevated in the skeletal muscle tissue of animals with trichinellosis. We suggest that the biological significance of this phenomenon might be associated with securing integrity of the newly formed nurse cell within the surrounding healthy skeletal muscle tissue. The increased sialylation might inhibit the affected muscle cell contractility through decreased membrane ion gating, helping the parasite accommodation process.

Keywords: glycosylation, sialic acid, nurse cell

Received: February 9, 2015; Accepted: July 1, 2015; Published online: September 7, 2015


References

  1. Aminoff D. 1961: Methods for the quantitative estimation of N-acetylneuraminic acid and their application to hydrolysates of sialomucoids. Biochem. J. 81: 384-392. Go to original source... Go to PubMed...
  2. Andrew C., Appel S.H. 1973: Macromolecular characterization of membranes: 1. Proteins and sialic acid of normal and denervated muscle. J. Biol. Chem. 248: 5156-5163. Go to PubMed...
  3. Babál P., Pindak F.F., Wells D.J., Gardner W.A. 1994: Purification and characterization of a sialic acid-specific lectin from Tritrichomonas mobilensis. Biochem. J. 299: 341-346. Go to original source... Go to PubMed...
  4. Barresi R., Campbell K.P. 2006: Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119: 199-207. Go to original source... Go to PubMed...
  5. Broccolini A., Gidaro T., De Cristofaro R., Morosetti R., Gliubizzi C., Ricci E., Tonali P.A., Mirabella M. 2008: Hyposialylation of neprilysin possibly affects its expression and enzymatic activity in hereditary inclusion-body myopathy muscle. J. Neurochem. 105: 971-981. Go to original source... Go to PubMed...
  6. Broccolini A., Gidaro T., Morosetti R., Sancricca C., Mirabella M. 2011: Hereditary inclusion-body myopathy with sparing the quadriceps: the many tiles of an incomplete puzzle. Acta Myol. 30: 91-95. Go to PubMed...
  7. Capó V., Despommier D.D. 1996: Clinical aspects of infection with Trichinella spp. Clin. Microbiol. Rev. 9: 47-54. Go to PubMed...
  8. Combs A.C., Ervasti J.M. 2005: Enhanced laminin binding by alpha-dystroglycan after enzymatic deglycosylation. Biochem. J. 390: 303-309. Go to original source... Go to PubMed...
  9. Cotrufo R., Appel S.H. 1973: Effects of denervation on glycoproteins of rabbit grastrocnemius and soleus muscle. Exp. Neurol. 39: 58-69. Go to original source... Go to PubMed...
  10. Cox M.L., Schray C.L., Luster C.N., Stewart Z.S., Korytko P.J., Khan K.N.M., Paulauskis J.D., Dunstan R.W. 2006: Assessment of fixatives, fixation, and tissue processing on morphology and RNA integrity. Exp. Mol. Pathol. 80: 183-191. Go to original source... Go to PubMed...
  11. Despommier D.D. 1998: How does Trichinella spiralis make itself home? Parasitol. Today 14: 318-323. Go to original source... Go to PubMed...
  12. Eisenberg I., Avidan N., Potikha T., Hochner H., Chen M., Olender T., Barash M., Shemesh M., Sadeh M., Grabov-Nardini G., Shmilevich .I, Friedmann A., Karpati G., Bradley W.C., Baumbach L., Lancet D., Asher E.B., Beckmann J.S., Argov Z., Mitrani-Rosenbaum S. 2001: The UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase gene is mutated in recessive hereditary inclusion body myopathy. Nature Genet. 29: 83-87. Go to original source... Go to PubMed...
  13. Ervasti J.M., Campbell K.P. 1993: A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell. Biol. 122: 809-823. Go to original source... Go to PubMed...
  14. Figarella-Branger D., Pellisier J.F., Bianco N., Karpati G. 1999: Sequence of expression of MyoD1 and various cell surface and cytoskeletal proteins in regenerating mouse muscle fibers following treatment with sodium dihydrogen phosphate. J. Neurol. Sci. 170: 151-160. Go to original source... Go to PubMed...
  15. Gruden-Movsesijan A., Ilic N., Sofronic-Milosavlievic L. 2002: Lectin-blot analyses of Trichinella spiralis muscle larvae excretory-secretory components. Parasitol. Res. 88: 1004-1007. Go to original source... Go to PubMed...
  16. Hanisch F., Weidemann W., Großmann M., Joshi P.R., Holzhausen H.J., Stoltenburg G., Weis J., Zierz S., Horstkorte R. 2013: Sialylation and muscle performance: Sialic acid is a marker of muscle ageing. PLoS ONE 8: e80520. Go to original source... Go to PubMed...
  17. Hayashi Y.K., Ogawa M., Tagawa K., Noguchi S., Ishihara T., Nonaka I., Arahata K. 2001: Selective deficiency of α-dystroglycan in Fukuyama-type congenital muscular dystrophy. Neurology 57: 115-12. Go to original source... Go to PubMed...
  18. Hinderlich S., Stache R., Zeitler R., Reutter W. 1997: A bifunctional enzyme catalyzes the first two steps in N-acetylneuraminic acid biosynthesis in rat liver: purification and characterization of the UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase. J. Biol. Chem. 272: 24313-24318. Go to original source... Go to PubMed...
  19. Horstkorte R., Nohring S., Wiechens N., Schwarzkopf M., Danker K., Retter W., Lucka L. 1999: Tissue expression and amino acid sequence of murine UDP-N-acetylglucosamine-2-epimerase/N-acetylmannosamine kinase. Eur. J. Biochem. 260: 923-927. Go to original source... Go to PubMed...
  20. Johnson D., Montpetit M.L., Stocker P.J., Bennett E.S. 2004: The sialic acid component of the β1 subunit modulates voltage-gated sodium channel function. J. Biol. Chem. 279: 44303-44310. Go to original source... Go to PubMed...
  21. Kaku H., Kaneko H., Minamihara N., Iwata K., Jordan E.T., Rojo M.A., Minani-Ishii N., Minami E., Hisajima S., Shibuya N. 2007: Elderberry bark lectins evolved to recognize Neu5Acα2,6Gal/GalNAc sequence from a Gal/GalNAc binding lectin through the substitution of amino-acid residues critical for the binding to sialic acid. J. Biochem. 142: 393-401. Go to original source... Go to PubMed...
  22. Kapel C.M.O., Gamble H.R. 2000: Infectivity, persistence, and antibody response to domestic and sylvatic Trichinella spp. in experimentally infected pigs. Int. J. Parasitol. 30: 215-221. Go to original source... Go to PubMed...
  23. Knibbs R.N., Goldstein I.J., Ratcliffe R.M., Shibuya N. 1991: Characterization of the carbohydrate binding specificity of the leucoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. J. Biol. Chem. 266: 83-88. Go to PubMed...
  24. Komandarev S., Mihov L., Hovorka I. 1986: Immunological studies on different Trichinella species. I. Antigenic characterization by means of linear immunoelectrophoresis. Helminthologia 21: 13-19.
  25. Marini M., Ambrosini S., Sarchielli E., Thyrion G.D.Z., Bonaccini L., Vannelli G.B., Sgambati E. 2014: Expression of sialic acids in human adult skeletal muscle tissue. Acta Histochem. 116: 926-935. Go to original source... Go to PubMed...
  26. Matsuo A., Wu Z., Nagano I., Takahashi Y. 2000: Five types of nuclei present in the capsule of Trichinella spiralis. Parasitology 121: 203-210. Go to original source... Go to PubMed...
  27. McDearmon E.L., Combs A.C., Ervasti J.M. 2003: Core 1 glycans on α-dystroglycan mediate laminin-induced acetylcholine receptor clustering but not laminin binding. J. Biol. Chem. 278: 44868-44873. Go to original source... Go to PubMed...
  28. Michele D.E., Barresi R., Kanagawa M., Saito F., Cohn R.D., Satz J.S., Dollar J., Nishino I., Kelley R.I., Somer H., Straub V., Mathews K.D., Moore S.A., Campbell K.P. 2002: Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418: 422-425. Go to original source... Go to PubMed...
  29. Milcheva R., Petkova S., Babál P. 2009a: Detection of O-glycosylated proteins from different Trichinella species muscle larvae total extracts. Helminthologia 46: 139-144. Go to original source...
  30. Milcheva R.S., Petkova S.L., Dubinský P., Hurniková Z., Babál P. 2009b: Glycosylation changes in different developmental stages of Trichinella. Biologia 64: 180-186. Go to original source...
  31. Morelle W., Haslam S.M., Morris H.R., Dell A. 2000: Characterization of the N-linked glycans of adult Trichinella spiralis. Mol. Biochem. Parasitol. 109: 171-177. Go to original source... Go to PubMed...
  32. Nakamura K., Tsukamoto Y., Hijiya N., Higuchi Y., Yano S., Yokoyama S., Kumamoto T., Moriyama M. 2010: Induction of GNE in myofibers after muscle injury. Pathobiology 77: 191-199. Go to original source... Go to PubMed...
  33. Ochoa J., Pallis C. 1980: Trichinella thrives in both oxidative and glycolytic human muscle fibres. J. Neurol. Neurosurg. Psychiatry 43: 281-282. Go to original source... Go to PubMed...
  34. Ross J., Benn A., Jonuschies J., Boldrin L., Muntoni F., Hewitt J.E., Brown S.C., Morgan J.E. 2012: Defects in glycosylation impair satellite stem cell function and niche composition in the muscles of the dystrophic large (myd) mouse. Stem Cells 30: 2330-2341. Go to original source... Go to PubMed...
  35. Sasaki T., Yamada H., Matsumura K., Shimizu T., Kobata A., Endo T. 1998: Detection of O-mannosyl glycans in rabbitskeletal muscle α-dystroglycan. Biochim. Biophys. Acta 1425: 599-606. Go to original source... Go to PubMed...
  36. Schauer R. 2004: Sialic acids: fascinating sugars in higher animals and man. Zoology 107: 49-64. Go to original source... Go to PubMed...
  37. Schauer R. 2009: Sialic acids as regulators of molecular and cellular interactions. Curr. Opin. Struct. Biol. 19: 1-8. Go to original source... Go to PubMed...
  38. Schwetz T.A., Norring N.A., Ednie A.R., Bennett E.S. 2011: Sialic acids attached to O-glycans modulate voltage-gated potassium channel gating. J. Biol. Chem. 286: 4123-4132. Go to original source... Go to PubMed...
  39. Sefarini-Cessi F. 1977: Sialyltransferase activity in regenerating rat liver. Biochem. J. 166: 381-386. Go to original source... Go to PubMed...
  40. Tajima Y., Uyama E., Go S., Sato C., Tao N., Kotani M., Hino H., Suzuki A., Sanai Y., Kitajima K., Sakuraba H. 2005: Distal myopathy with rimmed vacuoles: impaired O-glycan formation in muscular glycoproteins. Am. J. Pathol. 166: 1121-1130. Go to original source... Go to PubMed...
  41. Traving C., Schauer R. 1998: Structure, function and metabolism of sialic acids. Cell. Mol. Life Sci. 54: 1330-1349. Go to original source... Go to PubMed...
  42. Varki A. 1997: Sialic acids as ligands in recognition phenomena. FASEB J. 11: 248-255. Go to PubMed...
  43. Warren L. 1959: The thiobarbituric acid assay of sialic acids. J. Biol. Chem. 234: 1971-1975. Go to PubMed...
  44. Yao K., Ubuka T., Masuoka N., Kinuta M., Ikeda T. 1989: Direct determination of bound sialic acids in sialoglycoproteins by acidic ninhydrin reaction. Anal. Biochem. 197: 332-335. Go to original source... Go to PubMed...