Lectin-binding characterizes the healthy human skeletal muscle glycophenotype and identifies disease-specific changes in dystrophic muscle

Glycobiology

Volumn 27, Issue 12, 2017, Pages 1134-1143

  McMorran, Brian J ^a   Miceli, M Carrie ^b   Baum, Linda G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Disease specific; Human; Lectin; Muscle glycosylation; Muscular dystrophy; Skeletal muscle

Indexed keywords

AGGLUTININ; ALPHA DYSTROGLYCAN; GLYCAN; GLYCOPROTEIN; JACALIN; LAMININ; LECTIN; MAACKIA AMURENSIS AGGLUTININ; NARCISSUS PSEUDONARCISSUS AGGLUTININ; PEANUT AGGLUTININ; TRICOSANTHES JAPONICA AGGLUTININ I; UNCLASSIFIED DRUG; WISTERIA FLORIBUNDA AGGLUTININ; MUSCLE PROTEIN; NARCISSUS LECTIN; PLANT LECTIN;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GLYCOSYLATION; HISTOCHEMISTRY; HUMAN; HUMAN CELL; HUMAN TISSUE; LECTIN BINDING; MUSCULAR DYSTROPHY; MYOBLAST; MYOTUBE; PRIORITY JOURNAL; RECEPTOR BINDING; SKELETAL MUSCLE; CHEMISTRY; METABOLISM; NARCISSUS; PATHOLOGY; SKELETAL MYOBLAST; TRANSFORMED CELL LINE;

CELL LINE, TRANSFORMED; GLYCOPROTEINS; HUMANS; MUSCLE PROTEINS; MUSCULAR DYSTROPHIES; MYOBLASTS, SKELETAL; NARCISSUS; PLANT LECTINS;

EID: 85044325101     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwx073     Document Type: Article

References (59)

1. Briggs DC, Yoshida-Moriguchi T, Zheng T, Venzke D, Anderson ME, Strazzuli A, Moracci M, Yu L, Hohenester E, Campbell K.P. 2016. Structural basis of laminin binding to the LARGE glycans on dystroglycan. Nat Chem Biol. 12(10):810-814.
2. Bönnemann CG, Modi R, Noguchi S, Mizuno Y, Yoshida M, Gussoni E, McNally EM, Duggan DJ, Angelini C, Hoffman EP. 1995. Betasarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex. Nat Genet. 11(3):266-273.
3. Cabrera PV, Pang M, Marshall JL, Kung R, Nelson SF, Stalnaker SH, Wells L, Crosbie-Watson RH, Baum LG. 2012. High throughput screening for compounds that alter muscle cell glycosylation identifies new role for N-glycans in regulating sarcolemmal protein abundance and laminin binding. J Biol Chem. 287(27):22759-22770.
4. Campbell C, McMillan HJ, Mah JK, Tarnopolsky M, Selby K, McClure T, Wilson DM, Sherman ML, Escolar D, Attie KM. 2017. Myostatin inhibitor ACE-031 treatment of ambulatory boys with Duchenne muscular dystrophy: Results of a randomized, placebo-controlled clinical trial. Muscle Nerve. 55(4):458-464.
5. Campbell K.P, Kahl SD. 1989. Association of dystrophin and an integral membrane glycoprotein. Nature. 338(6212):259-262.
6. Capaldi MJ, Dunn MJ, Sewry CA, Dubowitz V. 1984a. Binding of Ricinus communis I lectin to the muscle cell plasma membrane in diseased muscle. J Neurol Sci. 64(3):315-324.
7. Capaldi MJ, Dunn MJ, Sewry CA, Dubowitz V. 1984b. Altered binding of Ricinus communis I lectin by muscle membranes in Duchenne muscular dystrophy. J Neurol Sci. 63(1):129-141.
8. Capaldi MJ, Dunn MJ, Sewry CA, Dubowitz V. 1985a. Lectin blotting of human muscle. Identification of a high molecular weight glycoprotein which is absent or altered in Duchenne muscular dystrophy. J Neurol Sci. 68(2-3):225-231.
9. Capaldi MJ, Dunn MJ, Sewry CA, Dubowitz V. 1985b. Lectin binding in human skeletal muscle: A comparison of 15 different lectins. Histochem J. 17(1):81-92.
10. Cummings RD, Kornfeld S. 1982. Characterization of the structural determinants required for the high affinity interaction of asparagine-linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J Biol Chem. 257(19):11230-11234.
11. Drysdale RG, Herrick PR, Franks D. 1968. The specificity of the haemagglutinin of the Castor bean, Ricinus communis. Vox Sang. 15(3):194-202.
12. Dunn MJ, Sewry CA, Dubowitz V. 1982. Cytochemical studies of lectin binding by diseased human muscle. J Neurol Sci. 55(2):147-159.
13. Ervasti JM, Campbell K.P. 1993. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol. 122(4):809-823.
14. Etzler ME, Gupta S, Borrebaeck C. 1981. Carbohydrate binding properties of th Dolichos biflorus lectin and its subunits. J Biol Chem. 256(5): 2367-2370.
15. Go S, Veillon L, Ciampa MG, Mauri L, Sato C, Kitajima K, Prinetti A, Sonnino S, Inokuchi JI. 2017. Altered expression of ganglioside GM3 molecular species and a potential regulatory role during myoblast differentiation. J Biol Chem. 292(17):7040-7051.
16. Greenaway PJ, LeVine D. 1973. Binding of N-acetyl-neuraminic acid by wheat-germ agglutinin. Nat New Biol. 241(110):191-192.
17. Guiraud S, Squire SE, Edwards B, Chen H, Burns DT, Shah N, Babbs A, Davies SG, Wynne GM, Russell AJ et al. 2015. Second-generation compound for the modulation of utrophin in the therapy of DMD. Hum Mol Genet. 24(15):4212-4224.
18. Gundry RL, Raginski K, Tarasova Y, Tchernyshyov I, Bausch-Fluck D, Elliott ST, Boheler KR, Van Eyk JE, Wollscheid B. 2009. The mouse C2C12 myoblast cell surface N-linked glycoproteome: Identification, glycosite occupancy, and membrane orientation. Mol Cell Proteomics. 8(11): 2555-2569.
19. Hara Y, Kanagawa M, Kunz S, Yoshida-Moriguchi T, Satz JS, Kobayashi YM, Zhu Z, Burden SJ, Oldstone MB, Campbell K.P. 2011. Likeacetylglucosaminyltransferase (LARGE)-dependent modification of dystroglycan at Thr-317/319 is required for laminin binding and arenavirus infection. Proc Natl Acad Sci USA. 108(42):17426-17431.
20. Hayashi YK, Chou FL, Engvall E, Ogawa M, Matsuda C, Hirabayashi S, Yokochi K, Ziober BL, Kramer RH, Kaufman SJ et al. 1998. Mutations in the integrin alpha7 gene cause congenital myopathy. Nat Genet. 19(1): 94-97.
21. Holmberg J, Durbeej M. 2013. Laminin-211 in skeletal muscle function. Cell Adh Migr. 7(1):111-121.
22. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell K.P. 1992. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature. 355 (6362):696-702.
23. Inamori K, Yoshida-Moriguchi T, Hara Y, Anderson ME, Yu L, Campbell K.P. 2012. Dystroglycan function requires xylosyl- and glucuronyltransferase activities of LARGE. Science. 335(6064):93-96.
24. Iwata Y, Suzuki O, Wakabayashi S. 2013. Decreased surface sialic acid content is a sensitive indicator of muscle damage. Muscle Nerve. 47(3):372-378.
25. Kaku H, Van Damme EJ, Peumans WJ, Goldstein IJ. 1990. Carbohydratebinding specificity of the daffodil (Narcissus pseudonarcissus) and amaryllis (Hippeastrum hybr.) bulb lectins. Arch Biochem Biophys. 279(2): 298-304.
26. Konami Y, Yamamoto K, Osawa T, Irimura T. 1994. Strong affinity of Maackia amurensis hemagglutinin (MAH) for sialic acid-containing Ser/ Thr-linked carbohydrate chains of N-terminal octapeptides from human glycophorin A. FEBS Lett. 342(3):334-338.
27. Lim KR, Maruyama R, Yokota T. 2017. Eteplirsen in the treatment of Duchenne muscular dystrophy. Drug Des Devel Ther. 11:533-545.
28. Lotan R, Skutelsky E, Danon D, Sharon N. 1975. The purification, composition, and specificity of the anti-T lectin from peanut (Arachis hypogaea). J Biol Chem. 250(21):8518-8523.
29. Mamchaoui K, Trollet C, Bigot A, Negroni E, Chaouch S, Wolff A, Kandalla PK, Marie S, Di Santo J, St Guily JL et al. 2011. Immortalized pathological human myoblasts: Towards a universal tool for the study of neuromuscular disorders. Skelet Muscle. 1:34.
30. Marshall JL, Kwok Y, McMorran BJ, Baum LG, Crosbie-Watson RH. 2013. The potential of sarcospan in adhesion complex replacement therapeutics for the treatment of muscular dystrophy. FEBS J. 280(17):4210-4229.
31. Marshall JL, Holmberg J, Chou E, Ocampo AC, Oh J, Lee J, Peter AK, Martin PT, Crosbie-Watson RH. 2012. Sarcospan-dependent Akt activation is required for utrophin expression and muscle regeneration. J Cell Biol. 197(7):1009-1027.
32. Mayer U, Saher G, Fässler R, Bonnemann A, Echtermeyer F, von der Mark N, Misoge N, Pöschl E, von der Mark K. 1997. Absence of integrin alpha 7 causes a novel form of muscular dystrophy. Nat Genet. 17(3):318-323.
33. McMorran BJ, McCarthy FE, Gibbs EM, Pang M, Marshall JL, Nairn AV, Moremen KW, Crosbie-Watson RH, Baum LG. 2016. Differentiationrelated glycan epitopes identify discrete domains of the muscle glycocalyx. Glycobiology. 26(10):1120-1132.
34. Mega T, Oku H, Hase S. 1992. Characterization of carbohydrate-binding specificity of concanavalin A by competitive binding of pyridylamino sugar chains. J Biochem. 111(3):396-400.
35. Mendell JR, Goemans N, Lowes LP, Alfano LN, Berry K, Shao J, Kave EM, Mercuri E, Eteplirsen Study Group and Telethon Foundation DMD Italian Network. 2016. Longitudinal effect of eteplirsen versus historical control on ambulation in Duchenne muscular dystrophy. Ann Neurol. 79(2):257-271.
36. Mizuno Y, Noguchi S, Yamamoto H, Yoshida M, Suzuki A, Hagiwara Y, Havashi YK, Arahata K, Nonaka I, Hira S et al. 1994. Selective defect of sarcoglycan complex in severe childhood autosomal recessive muscular dystrophy muscle. Biochem Biophys Res Commun. 203(2):979-983.
37. Nguyen HH, Javasinha V, Xia B, Hoyte K, Martin PT. 2002. Overexpression of the cytotoxic T cell GalNAc transferase in skeletal muscle inhibits muscular dystrophy in mdx mice. Proc Natl Acad Sci USA. 99(8):5616-5621.
38. Noguchi S, McNally EM, Ben Othmane K, Hagiwara Y, Mizuno Y, Yoshida M, Yamamoto H, Bönnemann CG, Gussoni E, Denton PH et al. 1995. Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy. Science. 270(5237):819-822.
39. Reinig AM, Mirzaei S, Berlau DJ. 2017. Advances in the treatment of duchenne muscular dystrophy: new and emerging pharmacotherapies. Pharmacotherapy. 37(4):492-499.
40. Ricotti V, Spinty S, Roper H, Hughes I, Tejura B, Robinson N, Layton G, Davies K, Muntoni F, Tinsley J. 2016. Safety, tolerability, and pharmacokinetics of SMT C1100, a 2-Arylbenzoxazole utrophin modulator, following single- and multiple-dose administration to pediatric patients with duchenne muscular dystrophy. PLoS One. 11(4):e0152840.
41. Rinderle SJ, Goldstein IJ, Matta KL, Ratcliffe RM. 1989. Isolation and characterization of amaranthin, a lectin present in the seeds of Amaranthus caudatus, that recognizes the T- (or cryptic T)-antigen. J Biol Chem. 264 (27):16123-16131.
42. Roberds SL, Leturcq F, Allamand V, Piccolo F, Jeanpierre M, Anderson RD, Lim LE, Lee JC, Tomé FM, Romero NB. 1994. Missense mutations in the adhalin gene linked to autosomal recessive muscular dystrophy. Cell. 78 (4):625-633.
43. Sanes JR, Cheney JM. 1982. Lectin binding reveals a synapse-specific carbohydrate in skeletal muscle. Nature. 300(5893):646-647.
44. Scott LJ, Bacou F, Sanes JR. 1988. A synapse-specific carbohydrate at the neuromuscular junction: Association with both acetylcholinesterase and a glycolipid. J Neurosci. 8(3):932-944.
45. Shibuya N, Goldstein IJ, Broekaert WF, Nsimba-Lubaki M, Peeters B, Peumans WJ. 1987. The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(alpha 2-6)Gal/GalNAc sequence. J Biol Chem. 262(4):1596-1601.
46. Thomas PJ, Xu R, Martin PT. 2016. B4GALNT2 (GALGT2) Gene Therapy Reduces Skeletal Muscle Pathology in the FKRP P448L Mouse Model of Limb Girdle Muscular Dystrophy 2I. Am J Pathol. 186(9):2429-2448.
47. Uchida T, Yamaizumi M, Mekada E, Okada Y, Tsuda M, Kurokawa T, Sugino Y. 1978. Reconstitution of hybrid toxin from Fragment A of diphtheria toxin and a subunit of Wistaria floribunda lectin. J Biol Chem. 253 (18):6307-6310.
48. Voit T, Sewry CA, Dunn MJ, Dubowitz V. 1988. Binding of Ricinus communis I lectin to developing dystrophic muscle in human fetus. J Neurol Sci. 84(2-3):301-314.
49. Wu AM, Wu JH, Lin LH, Lin SH, Liu JH. 2003. Binding profile of Artocarpus integrifolia agglutinin (Jacalin). Life Sci. 72(20):2285-2302.
50. Xia B, Hoyte K, Kammescheidt A, Deernick T, Ellisman M, Martin PT. 2002. Overexpression of the CT GalNAc transferase in skeletal muscle alters myofiber growth, neuromuscular structure, and laminin expression. Dev Biol. 242(1):58-73.
51. Xu R, Camboni M, Martin PT. 2007a. Postnatal overexpression of the CT GalNAc transferase inhibits muscular dystrophy in mdx mice without altering muscle growth or neuromuscular development: Evidence for a utrophin-independent mechanism. Neuromuscul Disord. 17(3): 209-220.
52. Xu R, DeVries S, Camboni M, Martin PT. 2009. Overexpression of Galgt2 reduces dystrophic pathology in the skeletal muscles of alpha sarcoglycan-deficient mice. Am J Pathol. 175(1):235-247.
53. Xu R, Chandrasekharan K, Yoon JH, Camboni M, Martin PT. 2007b. Overexpression of the cytotoxic T cell (CT) carbohydrate inhibits muscular dystrophy in the dyW mouse model of congenital muscular dystrophy 1A. Am J Pathol. 171(1):181-199.
54. Yamashita K, Umetsu K, Suzuki T, Ohkura T. 1992. Purification and characterization of a Neu5Ac alpha 2-<6Gal beta 1-<4GlcNAc and HSO3 (-)-<6Gal beta 1-
55. Yoon JH, Chandreasekharan K, Xu R, Glass M, Singhal M, Martin PT. 2009. The synaptic CT carbohydrate modulates binding and expression of extracellular matrix proteins in skeletal muscle: Partial dependence on utrophin. Mol Cell Neurosci. 41(4):448-463.
56. Yoshida-Moriguchi T, Campbell K.P. 2015. Matriglycan: A novel polysaccharide that links dystroglycan to the basement membrane. Glycobiology. 25(7):702-713.
57. Yoshida-Moriguchi T, Yu L, Stalnaker SH, Davis S, Kunz S, Madson M, Oldstone MB, Schachter H, Wells L, Campbell K.P. 2010. O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding. Science. 327(5961):88-92.
58. Young CS, Hicks MR, Ermolova NV, Nakano H, Jan M, Younesi S, Karumbayaram S, Kumagai-Cresse C, Wang D, Zack JA et al. 2016. A single CRISPR-Cas9 deletion strategy that targets the majority of DMD patients restores dystrophin function in hiPSC-derived muscle cells. Cell Stem Cell. 18(4):533-540.
59. Zhu CH, Mouly V, Cooper RN, Mamchoui K, Bigot A, Shay JW, Di Santo JP, Butter-Browne GS, Wright WE. 2007. Cellular senescence in human myoblasts is overcome by human telomerase reverse transcriptase and cyclin-dependent kinase 4: Consequences in aging muscle and therapeutic strategies for muscular dystrophies. Aging Cell. 6(4):515-523.