Skip to main content

Advertisement

SpringerLink
Log in

Purification of Two Novel Sugar Acid-binding Lectins from Haplomitrium Mnioides (bryophyte, Plantae) and their Preliminary Characterization

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Two novel sugar acid-binding lectins were purified from Haplomitrium mnioides (Lindb.) Schust. using a procedure consisting of ammonium sulfate precipitation, G-50 gel filtration, hydroxyapatite chromatography, and HW-50 gel filtration. We reported their partial physicochemical properties: molecular weight, affinity for carbohydrates and organic acids, pH stability, and dependence of their hemagglutination activity on metal ions. We also determined their N-terminal amino acid sequences. H. mnioides lectins (HMLs) were monomers (one with a molecular weight of approximately 27 kDa, and the other with a molecular weight of approximately 105 kDa) under both nonreducing and reducing conditions. They were named HML27 and HML105, respectively. Both HMLs had an affinity for N-acetylneuraminic acid, d-glucuronic acid, d-glucaric acid, bovine submaxillary mucin, heparin, and organic acids, such as citrate, 2-oxoglutaric acid, and d-2-hydroxyglutarate. Furthermore, HML27 had an affinity for α-d-galacturonic acid, d-malate, l-malate, and pyruvate, while HML105 had an affinity for d-gluconic acid. HML27 and HML105 are novel plant lectins: they have an affinity for sugar acids and organic acids and specifically recognize the carboxyl group, and there is no homology between their N-terminal amino acid sequences and those of the previously described lectins and agglutinins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AGL :

Aplysia depilans lectin

AS :

Ammonium sulfate

Asp :

Aspartic acid

BCA :

Bicinchoninic acid

BRA :

Semibalanus roseus agglutinin

BLAST :

Basic local alignment search tool

BSM :

Bovine submaxillary mucin

CS :

Chondroitin sulfate

CS2 :

Coli surface antigen

CV :

Column volume

D2HG :

d-2-Hydroxyglutarate

ECM :

Extracellular matrix

EDTA :

Ethylenediaminetetraacetic acid

Fuc :

Fucose

Gal :

Galactose

GalA :

Galacturonic acid

GalNAc :

N-acetyl-galactosamine

Glc :

Glucose

GlcA :

Glucuronic acid

GlcNAc :

N-acetyl-glucosamine

Glu :

Glutamic acid

GAG :

Glycosaminoglycan

HA :

Hemagglutination activity

HEL :

Hericium erinaceum lectin

HHL :

Human heparin lectin

HML :

Haplomitrium mnioides lectin

IDH :

Isocitrate dehydrogenase

IdoA :

Iduronic acid

IEW :

Ion-exchanged distilled water

KDM :

Histone lysine demethylase

Lac :

Lactose

LCA :

Lens culinaris agglutinin

MAA :

Maackia amurensis hemagglutinin

MAC :

Minimum agglutination concentration

MAL :

Maackia amurensis leukoagglutinin

Man :

Mannose

MLA-I :

Meretrix lusoria lectin

NANA :

N-Acetylneuraminic acid

PB :

Phosphate buffer

PHD :

Prolyl hydroxylase

PJA :

Paecilomyes japonica agglutinin

PSA :

Polyporus squamosus agglutinin

Rha :

Rhamnose

SAA :

Sialic acid-binding agglutinin

SBL-C :

Rana catesbeiana lectin

scorpion :

Heterometrus granulomanus lectin

SDS-PAGE :

Sodium dodecyl sulfate-polyaclylamidegel electrophoresis

SNA-I :

Sambucus nigra agglutinin

SPL-I :

Apostichopus japonicus lectin

TB :

Tris-HCl buffer

TET :

Ten–eleven translocation

TFL :

Tritrichomonas fetus lectin

TML :

Tritrichomonas mobilensis lectin

w/v :

Weight/volume

Xyl :

Xylose

References

  1. Ceri, H., Hwang, S. W., & Cheung, H. (1990). Endogenous heparin-binding lectin activity in human placenta: purification and developmental expression. Biochemistry and Cell Biology, 68, 790–795.

    Article  CAS  Google Scholar 

  2. Rutishauser, U., & Sachs, L. (1975). Cell-to-cell binding induced by different lectins. Journal of Cell Biology, 65, 247–257.

    Article  CAS  Google Scholar 

  3. Burger, M. M. (1971). Surface changes detected by lectins and implications for growth regulation in normal and in transformed cells. Biomembranes, 2, 247–270.

    Article  CAS  Google Scholar 

  4. Hajto, T., Hostanska, K., & Gabius, H. J. (1989). Modulatory potency of the β-galactoside-specific lectin from mistletoe extract (Iscador) on the host defense system in vivo in rabbits and patients. Cancer Research, 49, 4803–4808.

    CAS  Google Scholar 

  5. Ohno, Y. I., Hirai, K. I., Kanoh, T., Uchino, H., & Ogawa, K. (1982). Subcellular localization of hydrogen peroxide production in human polymorphonuclear leukocytes stimulated with lectins, phorbol myristate acetate, and digitonin: an electron microscopic study using CeCl3. Blood, 60, 1195–1202.

    CAS  Google Scholar 

  6. Gabius, H. J., Engelhardt, R., Casper, J., Reile, D., Schumacher, S., Schmoll, H. J., et al. (1985). Cell surface lectins of transplantable human teratocarcinoma cells: purification of a new mannan-specific endogenous lectin. Tumour Biology: the Journal of the International Society for Oncodevelopmental Biology and Medicine, 6, 145–156.

    CAS  Google Scholar 

  7. Yen, E. S., Mansfield, M. J., Levine, F. R., & Wallace, H. J. (1981). The prickly lettuce agglutinin. II. Immunobiological properties. International Archives of Allergy and Applied Immunology, 65, 445–450.

    Article  CAS  Google Scholar 

  8. Kolb, H., Oschilewski, M., Schwab, E., Greulich, B., Roos, P., & Kiesel, U. (1986). Suppression of low-dose streptozotocin-induced diabetes by immunomodulatory lectins. Diabetes Research, 3, 183–186.

    CAS  Google Scholar 

  9. Smith, W. W. (1940). Production of antibacterial agglutinins by carp and trout at 10°C. Proceedings of the Society for Experimental Biology and Medicine, 45, 726–729.

    Article  CAS  Google Scholar 

  10. Besancon, F., & Ankel, H. (1974). Inhibition of interferon action by plant lectins. Nature, 250, 784–786.

    Article  CAS  Google Scholar 

  11. Ito, M., & Barron, L. A. (1974). Inactivation of herpes simplex virus by concanavalin A. Journal of Virology, 13, 1312–1318.

    CAS  Google Scholar 

  12. Lin, J., Tserng, K., Chen, C., Lin, L., & Tung, T. (1970). Abrin and ricin: a new antitumor substances. Nature, 227, 292–293.

    Article  CAS  Google Scholar 

  13. Kim, M., Rao, V. M., Tweardy, J. D., Prakash, M., Galili, U., & Gorelik, E. (1993). Lectin-induced apoptosis of tumor cells. Glycobiology, 3, 447–553.

    Article  CAS  Google Scholar 

  14. Lorenc-Kubis, I., Morawiecka, B., Wieczorek, E., Wisniowska, J., Wierzba, E., & Ferens, M. (1981). Effects of lectins on enzymatic properties plant acid phosphatases and ribonucleases. In T. C. Bøg-Hansen (Ed.), Lectins: biology, biochemistry, clinical biochemistry. 1, Proceedings of 3rd Lectin Meeting, Copenhagen (pp. 169–178). Germany: Walter De Gruyter Inc.

    Google Scholar 

  15. Nitta, K., Oyama, F., Oyama, R., Sekiguchi, K., Kawauchi, H., Takayanagi, Y., et al. (1993). Ribonuclease activity of sialic acid-binding lectin from Rana catesbeiana eggs. Glycobiology, 3, 37–45.

    Article  CAS  Google Scholar 

  16. Nowell, C. P. (1960). Phytohemagglutinin: an initiator of mitosis in cultures of normal human leukocytes. Cancer Research, 20, 462–466.

    CAS  Google Scholar 

  17. Farnes, P., Barker, E. B., Brownhill, E. L., & Fanger, H. (1964). Mitogenic activity in Phytolacca americana (Pokeweed). The Lancet, 2, 1100–1101.

    Article  CAS  Google Scholar 

  18. Ceri, H., Shadle, P. J., Kobiler, D., & Barondes, S. H. (1979). Extracellular lectin and its glycosaminoglycan inhibitor in chick muscle cultures. Journal of Supramolecular Structure, 11, 61–67.

    Article  CAS  Google Scholar 

  19. Chowdhury, M., Sarkar, M., & Mendal, C. (1985). Identification and isolation of an agglutinin from uterus of rats. Biochemical and Biophysical Research Communications, 130, 1301–1307.

    Article  CAS  Google Scholar 

  20. Nitta, K., Ozaki, K., Ishikawa, M., Furusawa, S., Hosono, M., Kawauchi, H., et al. (1994). Inhibition of cell proliferation by Rana catesbeiana and Rana Japonica lectins belonging to the ribonuclease superfamily. Cancer Research, 54, 920–927.

    CAS  Google Scholar 

  21. Ahmed, H., Chatterjee, P. B., Kelm, S., & Schauer, R. (1986). Purification of a sialic acid-specific lectin from the Indian scorpion Heterometrus granulomanus. Biological Chemistry Hoppe-Seyler, 367, 501–506.

    Article  CAS  Google Scholar 

  22. Nowak, P. T., & Barondes, H. S. (1975). Agglutinin from Limulus polyphemus, purification with formalinized horse erythrocytes as the affinity adsorbent. Biochimica et Biophysica Acta, 393, 115–123.

    Article  CAS  Google Scholar 

  23. Amanai, K., Sakurai, S., & Ohtaki, T. (1990). Purification and characterization of haemagglutinin in the haemolymph of the silkworm, Bombyx mori. Comparative Biochemistry and Physiology. B. Comparative Biochemistry, 97, 471–476.

    Article  Google Scholar 

  24. Yamazaki, M., Esumi-Kurisu, M., Mizuno, D., Ogata, K., & Kamiya, H. (1983). Marine animal lectin-dependent tumor recognition by macrophages. Gann: Japanese Journal of Cancer Research, 74, 405–411.

    CAS  Google Scholar 

  25. Kamiya, H., & Ogata, K. (1982). Hemagglutinins in the acorn barnacle Balanus (Megabalanus) roseus: purification and partial characterization. Bulletin of the Japanese Society of Scientific Fisheries, 48, 1421–1425.

    Article  CAS  Google Scholar 

  26. Gilboa-Garber, N., Susswein, J. A., Mizrahi, L., & Avichezer, D. (1985). Purification and characterization of the gonad lectin of Aplysia depilans. FEBS Letters, 181, 267–270.

    Article  CAS  Google Scholar 

  27. Kamiya, H., & Shimizu, Y. (1981). A natural agglutinin inhibitable by D-galacturonic acid in the sea hare Aplysia eggs: characterization and purification. Bulletin of the Japanese Society of Scientific Fisheries, 47, 255–259.

    Article  CAS  Google Scholar 

  28. Kamiya, H., Muramoto, K., & Goto, R. (1990). Purification and characterization of a lectin from a marine sponge Halichondria panicea. Bulletin of the Japanese Society of Scientific Fisheries, 56, 1159.

    Article  Google Scholar 

  29. Matsui, T., Ozeki, Y., Suzuki, M., Hino, A., & Titani, K. (1994). Purification and characterization of two Ca2+-dependent lectins from coelomic plasma of sea cucumber, Stichopus japonicus. The Journal of Biochemistry, 116, 1127–1133.

    CAS  Google Scholar 

  30. Kim, H. J., Chung, R. S., & Jeune, H. K. (1990). Lectin from marine shells (IX): purification and carbohydrates specificities of a lectin, MLA-1, from the hemolymph of Meretrix lusoria. The Korean Journal of Biochemistry, 23, 328–334.

    CAS  Google Scholar 

  31. Broekaert, F. W., Nsimba-Lubaki, M., Peeters, B., & Peumans, J. W. (1984). A lectin from elder (Sambucus nigra L.) bark. The Biochemical Journal, 221, 163–169.

    Article  CAS  Google Scholar 

  32. Lam, S. K., & Ng, T. B. (2009). Novel galactonic acid-binding hexameric lectin from Hibiscus mutabilis seeds with antiproliferative and potent HIV-1 reverse transcriptase inhibitory activities. Acta Biochimica Polonica, 56, 649–654.

    CAS  Google Scholar 

  33. Rutherford, M. W., Dick, E. W., Cavins Jr., F. J., Dombrink-Kurtzman, A. M., & Slodki, E. M. (1986). Isolation and characterization of a soybean lectin having 4-O-methylglucuronic acid specificity. Biochemistry, 25, 952–958.

    Article  CAS  Google Scholar 

  34. Chan, Y. S., Wong, J. H., & Ng, T. B. (2011). A glucuronic acid binding leguminous lectin with mitogenic activity toward mouse splenocytes. Protein & Peptide Letters, 18, 194–202.

    Article  CAS  Google Scholar 

  35. Kawagishi, H., Mori, H., Uno, A., Kimura, A., & Chiba, S. (1994). A sialic acid-binding lectin from the mushroom Hericium erinaceum. FEBS Letters, 340, 56–58.

    Article  CAS  Google Scholar 

  36. Mo, H., Winter, C. H., & Goldstein, J. I. (2000). Purification and characterization of a Neu5Acα2-6Galβ1-4Glc/GlcNAc-specific lectin from the fruiting body of the polypore mushroom Polyporus squamosus. The Journal of Biological Chemistry, 275, 10623–10629.

    Article  CAS  Google Scholar 

  37. Potebnya, P. G., Tanasienko, A. O., Titova, P. G., Kovalenko, A. E., & Getman, I. E. (2002). Specificity and biological activity of cytotoxic lectins synthesized by Bacillus subtilis B-7025. Experimental Oncology, 24, 150–152.

    CAS  Google Scholar 

  38. Zipris, D., & Gilboa-Garber, N. (1987). Stimulation of human peripheral lymphocytes and induction of interleukin 2 production by a lectin from the gonad of the sea hare, Aplysia fasciata. Developmental and Comparative Immunology, 11, 501–511.

    Article  CAS  Google Scholar 

  39. Leibovici, J., Avichezer, D., & Gilboa-Garber, N. (1986). Effect of lectins on tumorigenicity of AKR lymphoma cells of varying malignancy. Anticancer Research, 6, 1411–1415.

    CAS  Google Scholar 

  40. Avichezer, D., Leibovici, J., Gilboa-Garber, N., & Michowitz, M. (1987). New galactophilic lectins reduce tumorigenicity and preserve immunogenicity of Lewis lung carcinoma cells. In K. Lapis & S. Eckhardt (Eds.), Lectures and Symposia 14th Int. Cancer Cong., II (pp. 79–85). Basel: Karger.

    Google Scholar 

  41. Nitta, K., Takayanagi, G., Kawauchi, H., & Hakomori, S. (1987). Isolation and characterization of Rana catesbeiana lectin and demonstration of the lectin-binding glycoprotein of rodent and human tumor cell membranes. Cancer Research, 47, 4877–4883.

    CAS  Google Scholar 

  42. Wang, W. C., & Cummings, R. D. (1988). The immobilized leukoagglutinin from the seeds of Maackia amurensis binds with high affinity to complex-type Asn-linked oligosaccharides containing terminal sialic acid-linked alpha-2,3 to penultimate galactose residues. The Journal of Biological Chemistry, 263, 4576–4585.

    CAS  Google Scholar 

  43. Bartholomew-Began, E. S. (1991). A morphogenetic re-evaluation of Haplomitrium Nees (Hepatophyta). Bryophytorum Bibliotheca, Bd. 41. J. Cramer, 1–297.

  44. Smith, M. G. (1955). Bryophytes and Pteridophytes. Cryptogamic botany (2nd ed.). New York: McGraw Hill.

    Google Scholar 

  45. Schuster, R. M. (1966). The Hepaticae and Anthocerotae of North America, (Vol. I). New York: Columbia University Press.

    Google Scholar 

  46. Schuster, R. M. (1967). Studies on Hepaticae XV. Calobryales. Nova Hedwigia, 13. J. Cramer 1–63.

  47. Forrest, L. L., Davis, E. C., Long, D. G., Crandall-Stotler, B. J., Clark, A., & Hollingsworth, M. L. (2006). Unraveling the evolutionary history of the Liverworts (Marchantiophyta): multiple taxa, genomes and analyses. The Bryologist, 109, 303–334.

    Article  CAS  Google Scholar 

  48. Qiu, Y. L., Li, L., Wang, B., Chen, Z., Knoop, V., Groth-Malonek, M., et al. (2006). The deepest divergences in land plants inferred from phylogenomic evidence. Proceedings of the National Academy of Sciences of the United States of America, 103, 15511–15516.

    Article  CAS  Google Scholar 

  49. Crandall-Stotler, B. J., Forrest, L. L., & Stotler, R. E. (2005). Evolutionary trends in the simple thalloid liverworts (Marchantiophyta, Jungermanniopsida subclass Metzgeriidae). Taxon, 54, 299–316.

    Article  Google Scholar 

  50. Adam, K. P., & Becker, H. (1993). A lectin from the liverwort Marchantia polymorpha L. Experientia, 49, 1098–1100.

    Article  CAS  Google Scholar 

  51. Peumans, W. J., Fouquaert, E., Jauneau, A., Rougé, P., Lannoo, N., Hamada, H., et al. (2007). The liverwort Marchantia polymorpha expresses orthologs of the fungal Agaricus bisporus agglutinin family. Plant Physiology, 144, 637–647.

    Article  CAS  Google Scholar 

  52. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., et al. (1985). Measurement of protein using bicinchoninic acid. Analytical Biochemistry, 150, 76–85.

    Article  CAS  Google Scholar 

  53. Hori, K., Miyazawa, K., & Ito, K. (1986). Preliminary characterization of agglutinins from seven marine algal species. Bulletin of the Japanese Society of Scientific Fisheries, 52, 323–331.

    Article  Google Scholar 

  54. Havelaar, A. C., Mancini, G. M. S., Beerens, C. E. M. T., Souren, R. M., & Verheijen, F. W. (1998). Purification of the lysosomal sialic acid transporter. The Journal of Biological Chemistry, 273, 34568–34574.

    Article  CAS  Google Scholar 

  55. Bisaccia, F., Indiveri, C., & Palmieri, F. (1988). Purification and reconstitution of two anion carriers from rat liver mitochondria: the dicarboxylate and the 2-oxoglutarate carrier. Biochimica et Biophysica Acta, 933, 229–240.

    Article  CAS  Google Scholar 

  56. Picault, N., Palmieri, L., Pisano, I., Hodges, M., & Palmieri, F. (2002). Identification of a novel transporter for dicarboxylates and tricarboxylates in plant mitochondria. The Journal of Biological Chemistry, 277, 24204–24211.

    Article  CAS  Google Scholar 

  57. Bisaccia, F., De Palma, A., & Palmieri, F. (1989). Identification and purification of the tricarboxylate carrier from rat liver mitochondria. Biochimica et Biophysica Acta, 977, 171–176.

    Article  CAS  Google Scholar 

  58. Walaszek, Z. (1990). Potential use of D-glucaric acid derivatives in cancer prevention. Cancer Letters, 54, 1–8.

    Article  CAS  Google Scholar 

  59. Health, Labour & Welfare Ministry. 2007. The Japanese Standards of Food Additives, 8th ed. Available from: http://www.mhlw.go.jp/seisakunitsuite/bunya/kenkou_iryou/shokuhin/syokuten/dl/8e03.pdf. Accessed Dec 2007.

  60. Nagels, L., Dongen, V. W., & Parmentier, F. (1982). Cestric acid, a caffeic acid ester from Cestrum euanthes. Phytochemistry, 21, 743–746.

    Article  CAS  Google Scholar 

  61. Strack, D., Engel, U., Weissenbӧck, G., Grotjahn, L., & Wray, V. (1986). Ferulic acid esters of sugar carboxylic acids from primary leaves of Rye (Secale cereale). Phytochemistry, 25, 2605–2608.

    Article  CAS  Google Scholar 

  62. Spínola, V., Pinto, J., & Castilho, C. P. (2015). Identification and quantification of phenolic compounds of selected fruits from Madeira Island by HPLC-DAD-ESI-MSn and screening for their antioxidant activity. Food Chemistry, 173, 14–30.

    Article  Google Scholar 

  63. Peumans, W. J., & Van Damme, E. J. (1995). The role of lectins in plant defence. The Histochemical Journal, 27, 253–271.

    Article  CAS  Google Scholar 

  64. Park, J. H., Ryu, C. S., Kim, H. N., Na, Y. J., Park, H. J., & Kim, H. (2004). A sialic acid-specific lectin from the mushroom Paecilomyces japonica that exhibits hemagglutination activity and cytotoxicity. Protein & Peptide Letters, 11, 563–569.

    Article  CAS  Google Scholar 

  65. Tronchin, G., Esnault, K., Sanchez, M., Larcher, G., Marot-Leblond, A., & Bouchara, J. P. (2002). Purification and partial characterization of a 32-kilodalton sialic acid-specific lectin from Aspergillus fumigatus. Infection and Immunity, 70, 6891–6895.

    Article  CAS  Google Scholar 

  66. Babál, P., Pindak, F. F., Wells, D. J., & Gardner Jr., W. A. (1994). Purification and characterization of a sialic acid-specific lectin from Tritrichomonas mobilensis. The Biochemical Journal, 299, 341–346.

    Article  Google Scholar 

  67. Babál, P., Pindak, F. F., Russell, L. C., & Gardner Jr., W. A. (1999). Sialic acid-specific lectin from Tritrichomonas foetus. Biochimica et Biophysica Acta, General Subjects, 1428, 106–116.

    Article  Google Scholar 

  68. Sjoberg, P. O., Lindahl, M., Porath, J., & Wadstrom, T. (1988). Purification and characterization of CS2, a sialic acid-specific haemagglutinin of enterotoxigenic Escherichia coli. Biochemical Journal, 255, 105–111.

    Article  CAS  Google Scholar 

  69. Takahashi, T., Ramachandramurthy, P., & Liener, I. E. (1967). Some physical and chemical properties of a phytohemagglutinin isolated from Phaseolus vulgaris. Biochimica et Biophysica Acta, Protein Structure, 133, 123–133.

    Article  CAS  Google Scholar 

  70. Pusztai, A., Grant, G., & Stewart, J. C. (1981). A new type of Phaseolus vulgaris (cv. Pinto III) seed lectin: isolation and characterization. Biochimica et Biophysica Acta Protein Structure, 671, 146–154.

    Article  CAS  Google Scholar 

  71. Pratt, R. C., Singh, N. K., Shade, R. E., Murdock, L. L., & Bressan, R. A. (1990). Isolation and partial characterization of a seed lectin from tepary bean that delays bruchid beetle development. Plant Physiology, 93, 1453–1459.

    Article  CAS  Google Scholar 

  72. Sharma, A., Wong, J. H., Lin, P., Chan, Y. S., & Ng, T. B. (2010). Purification and characterization of a lectin from the Indian cultivar of French bean seeds. Protein & Peptide Letters, 17, 221–227.

    Article  CAS  Google Scholar 

  73. Lane, B. G., Dunwell, J. M., Ray, J. A., Schmitt, M. R., & Cuming, A. C. (1993). Germin, a protein marker of early plant development, is an oxalate oxidase. The Journal of Biological Chemistry, 268, 12239–12242.

    CAS  Google Scholar 

  74. Lane, B. G. (1994). Oxalate, germin, and the extracellular matrix of higher plants. The FASEB Journal, 8, 294–301.

    CAS  Google Scholar 

  75. Dunwell, J. M., Khuri, S., & Gane, P. J. (2000). Microbial relatives of the seed storage proteins of higher plants: conservation of structure and diversification of function during evolution of the cupin superfamily. Microbiology and Molecular Biology Reviews, 64, 153–179.

    Article  CAS  Google Scholar 

  76. Nakata, M., Watanabe, Y., Sakurai, Y., Hashimoto, Y., Matsuzaki, M., Takahashi, Y., et al. (2004). Germin-like protein gene family of a moss, Physcomitrella patens, phylogenetically falls into two characteristic new clades. Plant Molecular Biology, 56, 381–395.

    Article  CAS  Google Scholar 

  77. Carafa, A., Duckett, G. J., & Ligrone, R. (2003). Subterranean gametophytic axes in the primitive liverwort Haplomitrium harbour a unique type of endophytic association with aseptate fungi. New Phytologist, 160, 185–197.

    Article  Google Scholar 

  78. Kottke, I., & Nebel, M. (2005). The evolution of mycorrhiza-like associations in liverworts: an update. New Phytologist, 167, 330–334.

    Article  CAS  Google Scholar 

  79. Mandal, C., & Mandal, C. (1990). Sialic acid binding lectins. Experientia, 46, 433–441.

    Article  CAS  Google Scholar 

  80. Gabius, H. J. (1997). Animal lectins. European Journal of Biochemistry, 243, 543–576.

    Article  CAS  Google Scholar 

  81. Lehmann, F., Tiralongo, E., & Tiralongo, J. (2006). Sialic acid-specific lectins: occurrence, specificity and function. Cellular and Molecular Life Sciences, 63, 1331–1354.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by MEXT-Supported Program for the Strategic Research Foundation at Private Universities. We would like to thank Naoko Norioka for her help.

Author information

Authors and Affiliations

  1. Division of Cell Recognition Study, Institute of Molecular Biomembrane and Glycobiology, Tohoku Pharmaceutical University, 4-4-1 Komatsushima, Aoba-ku, Sendai, 981-8558, Japan

    Hiroaki Masuzaki, Masahiro Hosono & Kazuo Nitta

Authors
  1. Hiroaki Masuzaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masahiro Hosono
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazuo Nitta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroaki Masuzaki.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Masuzaki, H., Hosono, M. & Nitta, K. Purification of Two Novel Sugar Acid-binding Lectins from Haplomitrium Mnioides (bryophyte, Plantae) and their Preliminary Characterization. Appl Biochem Biotechnol 181, 65–82 (2017). https://doi.org/10.1007/s12010-016-2199-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-016-2199-0

Keywords

Search

Navigation