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Biochemistry (Moscow)

, Volume 80, Issue 7, pp 820–835 | Cite as

Hypotheses of the origin of natural antibodies: A glycobiologist’s opinion

  • N. R. KhasbiullinaEmail author
  • N. V. Bovin
Review

Abstract

It is generally accepted that the generation of antibodies proceeds due to immunization of an organism by alien antigens, and the level and affinity of antibodies are directly correlated to the presence of immunogen. At the same time, vast experimental material has been obtained providing evidence of antibodies whose level remains unchanged and affinity is constant during a lifetime. In contrast to the first, adaptive immunoglobulins, the latter are named natural antibodies (nAbs). The nAbs are produced by B1 cells, whereas adaptive Abs are produced by B2. This review summarizes general data on nAbs and presents in more detail data on antigens of carbohydrate origin. Hypotheses on the origin of nAbs and their activation mechanisms are discussed. We present our thoughts on this matter supported by our experimental data on nAbs to glycans.

Keywords

natural antibodies B1 cells bacterial antigens autoantibodies polysaccharides molecular patterns DAMP 

Abbreviation

DAMP

damage-associated molecular patterns

mAbs

monoclonal antibodies

MAMP

microorganism-associated molecular patterns

nAbs

natural antibodies

TACA

tumor-associated carbohydrate antigens

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References

  1. 1.
    Winau, F., Westphal, O., and Winau, R. (2004) Paul Ehrlich- in search of the magic bullet, Microbes Infect., 68, 786–789.Google Scholar
  2. 2.
    Roit, A. (1991) Fundamentals of Immunology [Russian translation], Mir, Moscow.Google Scholar
  3. 3.
    Abelev, G. I. (1996) Fundamentals of immunity, Soros Educat. J., 5, 4–10.Google Scholar
  4. 4.
    Landsteiner, K., and Philip Miller, C. Ph., Jr. (1925) Serological studies on the blood of the primates. II. The blood groups in anthropoids apes, J. Exp. Med., 42, 853–862.PubMedCentralPubMedGoogle Scholar
  5. 5.
    Landsteiner, K., and Levine, P. (1927) Further observations on individual differences of human blood, Proc. Soc. Exp. Biol., 24, 941–942.Google Scholar
  6. 6.
    Burnet, F. M. (1976) A modification of Jerne’s theory of antibody production using the concept of clonal selection, CA Cancer J. Clin., 26, 119–121.PubMedGoogle Scholar
  7. 7.
    Silverstein, A. M. (2009) A History of Immunology, Academic Press, N. Y, 2nd Edn.Google Scholar
  8. 8.
    Burnet, F. M. (1978) Clonal selection and after, in Theoretical Immunology (Bell, G. I., Perelson, A. S., and Pimbley, G. H., Jr., eds.) Marcel Dekker Inc., pp. 63–85.Google Scholar
  9. 9.
    Yarilin, A. A. (2010) Immunology [in Russian], GEOTARMedia, Moscow.Google Scholar
  10. 10.
    Janeway, Ch. A., Travers, P., Jr., Walport, M., and Shlomchik, M. J. (2001) The Immune System in Health and Disease. Immunobiology, 5th Edn., Garland Science, N. Y.Google Scholar
  11. 11.
    Schatz, D. G., Oettinger, M. A., and Baltimore, D. (1989) The V(D)J recombination activating gene, RAG-1, Cell, 59, 1035–1048.PubMedGoogle Scholar
  12. 12.
    Lutz, H. U. (2012) Naturally occurring antibodies (nAbs), Adv. Exp. Med. Biol., 750, vii-x, p. 267.Google Scholar
  13. 13.
    Hayakawa, K., and Hardy, R. R. (2000) Development and function of B-1 cells, Curr. Opin. Immunol., 12, 346–353.PubMedGoogle Scholar
  14. 14.
    Guilbert, B., Digheiro, G., and Avrameas, S. (1982) Naturally occurring antibodies against nine common antigens in human sera, J. Immunol., 128, 2779–2787.PubMedGoogle Scholar
  15. 15.
    Zhou, Z-H., Tzioufas, G. A., and Notkins, A. L. (2007) Properties and function of polyreactive antibodies and polyreactive antigen-binding B cells, J. Autoimmun., 29, 219–228.PubMedCentralPubMedGoogle Scholar
  16. 16.
    Cohen, I. (2013) Autoantibody repertoires, natural biomarkers, and system controllers, Trends Immunol., 34, 620–625.PubMedGoogle Scholar
  17. 17.
    Daniels, G. (2003) Human Blood Groups, 3rd Edn., Blackwell Science, Oxford.Google Scholar
  18. 18.
    Gershvin, M. E., Meroni, P. L., and Shoenfeld, Y (2006) Autoantibodies, 2nd Edn., Elsevier Science.Google Scholar
  19. 19.
    Avrameas, S. (1991) Natural autoantibodies: from “horror autotoxicus” to “gnothiseauton”, Immunol. Today, 12, 154–159.PubMedGoogle Scholar
  20. 20.
    Boes, M. (2000) Role of natural and immune IgM antibodies in immune responses, Mol. Immunol., 37, 1141.1149.PubMedGoogle Scholar
  21. 21.
    Zhou, Z-H., Zhang, Y., Hu, Y-F., Wahl, L. M., Cisar, J. O., and Notkins, A. L. (2007) The broad antibacterial activity of the natural antibody repertoire is due to polyreactive antibodies, Cell Host Microbe, 1, 51–61.PubMedCentralPubMedGoogle Scholar
  22. 22.
    Racine, R., and Winslow, G. M. (2009) IgM in microbial infections: taken for granted? Immunol. Lett., 125, 79–85.PubMedCentralPubMedGoogle Scholar
  23. 23.
    Ochsenbein, A. F., Fehr, T, Lutz, C., Suter, M., Brombacher, F., Hengartner, H., and Zinkernagel, R. M. (1999) Control of early viral and bacterial distribution and disease by natural antibodies, Science, 286, 2156–2159.PubMedGoogle Scholar
  24. 24.
    Ochsenbein, A. F., and Zinkernagel, R. M. (2000) Natural antibodies and complement link innate and acquired immunity, Immunol. Today, 21, 624–630.PubMedGoogle Scholar
  25. 25.
    Baumgarth, N., Tung, J. W., and Herzenberg, L. A. (2005) Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion, Springer Semin. Immun., 26, 347–362.Google Scholar
  26. 26.
    Chou, M.-Y., Fogelstrand, L., Hartvigsen, K., Hansen, L. F., Woelkers, D., Shaw, P. X., Choi, J., Perkmann, T, Backhed, F., Miller, Y I., Horkko, S., Corr, M., Witztum, J. L., and Binder, C. J. (2009) Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans, J. Clin. Invest., 199, 1335–1349.Google Scholar
  27. 27.
    Lutz, H. U. (2007) Homeostatic roles of naturally occurring antibodies: an overview, J. Autoimmun., 29, 287–294.PubMedGoogle Scholar
  28. 28.
    Binder, C. J., Shaw, P. X., Chang, M.-K., Boullier, A., Hartvigsen, K., Horkko, S., Miller, Y I., Woelkers, D. A., Corr, M., and Witztum, J. L. (2005) The role of natural antibodies in atherogenesis, J. Lipid Res., 46, 1353–1363.PubMedGoogle Scholar
  29. 29.
    Tsiantoulas, D., Gruber, S., and Binder, C. J. (2013) B-1 cell immunoglobulin directed against oxidation-specific epitopes, Front. Immunol., 9, 415..Google Scholar
  30. 30.
    Galili, U. (2004) Immune response, accommodation, and tolerance to transplantation carbohydrate antigens, Transplantation, 78, 1093–1098.PubMedGoogle Scholar
  31. 31.
    Hayakawa, K., Hardy, R. R., and Herzenberg, L. A. (1986) Peritoneal Ly-1 B cells: genetic control, autoantibody production, increased lambda light chain expression, Eur. J. Immunol., 16, 450–456.PubMedGoogle Scholar
  32. 32.
    Bendelac, A., Bonneville, M., and Kearney, J. F. (2001) Autoreactivity by design: innate B and T lymphocytes, Nature Rev. Immunol., 1, 177–186.Google Scholar
  33. 33.
    Hayakawa, K., Asano, M., Shinton, S. A., Gui, M., Allman, D., Stewart, C. L., Silver, J., and Hardy, R. R. (1999) Positive selection of natural autoreactive B cells, Science, 285, 113–116.PubMedGoogle Scholar
  34. 34.
    Hao, Z., and Rajewsky, K. (2001) Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow, J. Exp. Med., 194, 1151–1163.PubMedCentralPubMedGoogle Scholar
  35. 35.
    Itakura, A., Szczepanik, M., Campos, R. A., Paliwal, V., Majewska, M., Matsuda, H., Takatsu, K., and Askenase, P. W. (2005) An hour after immunization peritoneal B-1 cells are activated to migrate to lymphoid organs where within 1 day they produce IgM antibodies that initiate elicitation of contact sensitivity, J. Immunol., 175, 7170–7178.PubMedGoogle Scholar
  36. 36.
    Abelev, G. L. (1971) Alpha-fetoprotein in ontogenesis and its association with malignant tumors, Adv. Cancer Res., 14, 295–358.PubMedGoogle Scholar
  37. 37.
    Barak, V. (2006) Tumor Biology. Tumor Markers, Tumor Targeting and Translational Cancer Research (Stigbrand, T, ed.) Karger Medical and Scientific Publishers, N.Y, p. 116.Google Scholar
  38. 38.
    Armenti, V. T, Moritz, M. J., Cardonick, E. H., and Davison, J. M. (2002) Immunosuppression in pregnancy: choices for infant and maternal health, Drugs, 62, 2361.2375.PubMedGoogle Scholar
  39. 39.
    Elliott, A. B., and Chakravarty, E. F. (2010) Immunosuppressive medications during pregnancy and lactation in women with autoimmune diseases, Womens Health (London), 6, 431–440.Google Scholar
  40. 40.
    Badami, K. G., Vanhecke, C., and Bingham, J. (2009) Maternal IgM anti-D, borderline foetal Doppler middle cerebral artery velocities and absent neonatal hemolysis, Transfus. Med., 19, 146–147.PubMedGoogle Scholar
  41. 41.
    Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K., and Walter, P. (2002) Molecular Biology of the Cell, 4th Edn., Garland Science, N.Y.Google Scholar
  42. 42.
    Mackie, R. I., Sghir, A., and Gaskins, H. R. (1999) Developmental microbial ecology of the neonatal gastrointestinal tract, Am. J. Clin. Nutr., 69, 1035–1045.Google Scholar
  43. 43.
    Mariat, D., Firmesse, O., Levenez, F., Guimaraes, V. D., Sokol, H., Dore, J., Corthier, G., and Furet, J.-P. (2009) The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age, BMC Microbiol., 9, 1–6.Google Scholar
  44. 44.
    Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R., and Gordon, J. I. (2008) Worlds within worlds: evolution of the vertebrate gut microbiota, Nature Rev. Microbiol., 6, 7767–7788.Google Scholar
  45. 45.
    Dethlefsen, L., Eckburg, P. B., Bik, E. M., and Relman, D. A. (2006) Assembly of the human intestinal microbiota, Trends Ecol. Evol., 21, 517–523.PubMedGoogle Scholar
  46. 46.
    Lanning, D. K., Rhee, K. J., and Knight, K. L. (2005) Intestinal bacteria and development of the B-lymphocyte repertoire, Trends Immunol., 26, 419–425.PubMedGoogle Scholar
  47. 47.
    Bulatova, E. M., and Bogdanova, N. M. (2010) The importance of the intestinal microbiota and probiotics in generation of immune response and health of a child, Vorp. Sovrem. Pediatr., 6, 37–44.Google Scholar
  48. 48.
    Berg, R. D. (1999) Bacterial translocation from the gastrointestinal tract, Adv. Exp. Med. Biol., 473, 11–30.PubMedGoogle Scholar
  49. 49.
    Kelly, D., King, T., and Aminov, R. (2007) Importance of microbial colonization of the gut in early life to the development of immunity, Mutat. Res., 622, 58–69.PubMedGoogle Scholar
  50. 50.
    Cash, H. L., and Hooper, L. V. (2005) Commensal bacteria shape intestinal immune system development, ASM News, 71, 77–83.Google Scholar
  51. 51.
    Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L., and Gordon, J. I. (2011) Human nutrition, the gut microbiome and the immune system, Nature, 474, 327–336.PubMedCentralPubMedGoogle Scholar
  52. 52.
    Otter, J. A., Vickery, K., Walker, J. T, de Lancey, P. E., Stoodley, P., Goldenberg, S. D., Salkeld, J. A., Chewins, J., Yezli, S., and Edgeworth, J. D. J. (2015) Surface-attached cells, biofilms and biocide susceptibility: implications for hospital cleaning and disinfection, Hosp. Infect., 89, 16–27.Google Scholar
  53. 53.
    Leid, J. G., Willson, C. J., Shirtliff, M. E., Hassett, D. J., Parsek, M. R., and Jeffers, A. K. (2005) The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing, J. Immunol., 175, 7512–7518.PubMedGoogle Scholar
  54. 54.
    Suzuki, K., Ha, S-A., Tsuji, M., and Fagarasan, S. (2007) Intestinal IgA synthesis: a primitive form of adaptive immunity that regulates microbial communities in the gut, Semin. Immunol., 19, 127–135.PubMedGoogle Scholar
  55. 55.
    Cerutti, A., and Rescigno, M. (2008) The biology of intestinal immunoglobulin A responses, Immunity, 28, 740–750.PubMedCentralPubMedGoogle Scholar
  56. 56.
    Tsuji, M., Suzuki, K., Kinoshita, K., and Fagarasan, S. (2008) Dynamic interactions between bacteria and immune cells leading to intestinal IgA synthesis, Semin. Immunol., 20, 59–66.PubMedGoogle Scholar
  57. 57.
    Deplancke, B., and Gaskins, H. R. (2001) Microbial modulation of innate defense: goblet cells and the intestinal mucus layer, Am. J. Clin. Nutr., 73, 1131–1141.Google Scholar
  58. 58.
    Frederiksen, R. F., Paspaliari, D. K., Larsen, T, Storgaard, B. G., Larsen, M. H., Ingmer, H., Palcic, M. M., and Leisner, J. J. (2013) Bacterial chitinases and chitin-binding proteins as virulence factors, Microbiology, 159, 833–847.PubMedGoogle Scholar
  59. 59.
    Langhendries, J. P. (2005) Early bacterial colonization of the intestine: why it matters, Ital. J. Pediatr., 31, 360–369.Google Scholar
  60. 60.
    Wold, A. E., and Adlerberth, I. (2000) Breast feeding and the intestinal microflora of the infant-implications for protection against infectious diseases, Adv. Exp. Med. Biol., 478, 77–93.PubMedGoogle Scholar
  61. 61.
    Lu, L., and Walker, W A. (2001) Pathologic and physiologic interactions of bacteria with the gastrointestinal epithelium, Am. J. Clin. Nutr., 73, 1124–1130.Google Scholar
  62. 62.
    Panigrahi, P., Parida, S., Pradhan, L., Mohapatra, S. S., Misra, P. R., Johnson, J. A., Chaudhry, R., Taylor, S., Hansen, N. I., and Gewolb, I. H. (2008) Long-term colonization of a Lactobacillus plantarum synbiotic preparation in the neonatal gut, J. Pediatr. Gastroenterol. Nutr., 47, 4553..Google Scholar
  63. 63.
    Abreu, M. T (2010) Toll-like receptor signaling in the intestinal epithelium: how bacterial recognition shapes intestinal function, Nature Rev. Immunol., 10, 131–144.Google Scholar
  64. 64.
    Guarner, F., and Malagelada, J.-R. (2003) Gut flora in health and disease, Lancet, 361, 512–519.PubMedGoogle Scholar
  65. 65.
    Balzan, S., Almeida Quadros, A., de Cleva, R., Zilberstein, B., and Cecconello, I. (2007) Bacterial translocation: overview of mechanisms and clinical impact, J. Gastroenterol. Hepatol., 22, 464–471.PubMedGoogle Scholar
  66. 66.
    Springer, G. F., Horton, R. E., and Forbes, M. (1959) Origin of antihuman blood group B agglutinins in germfree chicks, J. Exp. Med., 110, 221–244.PubMedCentralPubMedGoogle Scholar
  67. 67.
    Springer, G. F. (1971) Blood-group and Forssman antigenic determinants shared between microbes and mammalian cells, Prog. Allergy, 15, 9–77.PubMedGoogle Scholar
  68. 68.
    Wagner, R. D. (2008) Effects of microbiota on GI health: gnotobiotic research, Adv. Exp. Med. Biol., 635, 41–56.PubMedGoogle Scholar
  69. 69.
    De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J. B., Massart, S., Collini, S., Pieraccini, G., and Lionetti, P (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa, Proc. Natl. Acad. Sci. USA, 107, 14691–14696.PubMedCentralPubMedGoogle Scholar
  70. 70.
    Bischof, S. C. (2011) “Gut health”: a new objective in medicine? BMC Medicine, 9, 1–14.Google Scholar
  71. 71.
    Bos, N. A., Kimura, H., Meeuwsen, C. G., De Vi sser, H., Ha zenberg, M. P., Wostmannn, B. S., Pleasants, J. R., Benner, B., and Marcus, D. M. (1980) Serum immunoglobulin levels and naturally occurring antibodies against carbohydrate antigens in germ-free BALB/c mice fed chemically defined ultrafiltered diet, Eur. J. Immunol., 19, 2335–2339.Google Scholar
  72. 72.
    Kozakova, H., Kolinska, J., Lojda, Z., Rehakova, Z., Sinkora, J., Zakostelecka, M., Splichal, I., and Tlaskalova- Hogenova, E. (2006) Effect of bacterial monoassociation on brush-border enzyme activities in ex-germ-free piglets: comparison of commensal and pathogenic Escherichia coli strains, Microbes Infect., 8, 2629–2639.PubMedGoogle Scholar
  73. 73.
    Butler, J. E., Sun, J., Weber, P, Navarro, P., and Francis, D. (2000) Antibody repertoire development in fetal and newborn piglets. III. Colonization of the gastrointestinal tract selectively diversifies the preimmune repertoire in mucosal lymphoid tissues, Immunology, 100, 119–130.PubMedCentralPubMedGoogle Scholar
  74. 74.
    Coutinho, A., Kazatchkine, M. D., and Avrameas, S. (1995) Natural autoantibodies, Curr. Opin. Immunol., 7, 812–818.PubMedGoogle Scholar
  75. 75.
    Nores, G. A., Lardone, R. D., Comin, R., Alaniz, M. E., Moyano, A. L., and Irazoqui, F. J. (2008) Anti-GM1 antibodies as a model of the immune response to self-glycan, BBA, 1780, 538–545.PubMedGoogle Scholar
  76. 76.
    Danussi, C., Coslovi, A., Campa, C., Mucignat, M. T., Spessotto, P., Uggeri, F., Paoletti, S., and Colombatti, A. (2009) A newly generated functional antibody identifies Tn antigen as a novel determinant in the cancer cell-lymphatic endothelium interaction, Glycobiology, 19, 1056–1067.PubMedCentralPubMedGoogle Scholar
  77. 77.
    Mouthon, L., Haury, M., Lacroix-Desmazes, S., Barreau, C., Coutinho, A., and Kazatchkine, M. D. (1995) Analysis of the normal human IgG antibody repertoire, J. Immunol., 154, 5769–5778.PubMedGoogle Scholar
  78. 78.
    Hayakawa, K., and Hardy, R. R. (2005) Development of B cells producing natural autoantibodies to thymocytes and senescent erythrocytes, Springer Semin. Immun., 26, 363–375.Google Scholar
  79. 79.
    Lacroix-Desmazes, S., Srini, U., Kaveri, V., Mouthon, L., Ayouba, A., Malanchere, E., Coutinho, A., and Kazatchkine, M. D. (1998) Self-reactive antibodies natural autoantibodies in healthy individuals, J. Immunol. Methods, 216, 117–137.PubMedGoogle Scholar
  80. 80.
    Pancer, Z., and Cooper, M. D. (2006) The evolution of adaptive immunity, Annu. Rev. Immunol., 24, 497–518.PubMedGoogle Scholar
  81. 81.
    Servettaz, A., Guilpain, P, Tamas, N., Kaveri, S. V., Camoin, L., and Mouthon, L. (2008) Natural antiendothelial cell antibodies, Autoimmun. Rev., 7, 426–430.PubMedGoogle Scholar
  82. 82.
    Ronda, N., Haury, M., Nobrega, A., Kaveri, S. V., Coutlnho, A., and Kazatchkine, M. D. (1994) Analysis of natural and disease-associated autoantibody repertoires: anti-endothelial cell IgG autoantibody activity in the serum of healthy individuals and patients with systemic lupus erythematosus, Int. Immunol., 6, 1651–1660.PubMedGoogle Scholar
  83. 83.
    Pashov, A., Kenderov, A., Kyurkchiev, S., Kehayov, I., Hristova, S., Lacroix-Desmazes, S., Giltiay, N., Varamballi, S., Kazatchkine, M. D., and Kaveri, S. V. (2002) Autoantibodies to heat shock protein 90 in the human natural antibody repertoire, Int. Immunol., 14, 453–461.PubMedGoogle Scholar
  84. 84.
    Yadin, O., Sarov, B., Naggan, L., Slor, H., and Shoenfeld, Y. (1989) Natural autoantibodies in the serum of healthy women- a five-year follow-up, Clin. Exp. Immunol., 75, 402–406.PubMedCentralPubMedGoogle Scholar
  85. 85.
    Pierson, R. N., Loyd, J. E., Goodwin, A., Majors, D., Dummer, J. S., Mohacsi, P., Wheeler, A., Bovin, N., Miller, G. G., Olson, S., Johnson, J., Rieben, R., and Azimzadeh, A. (2002) Successful management of an ABOmismatched lung allograft using antigen-specific immunoadsorption, complement inhibition, and immunomodulatory therapy, Transplantation, 15, 79–84.Google Scholar
  86. 86.
    Wardemann, H., Yurasov, S., Schaefer, A., Young, J. W, Meffre, E., and Nussenzweig, M. C. (2003) Predominant autoantibody production by early human B cell precursors, Science, 301, 1374–1377.PubMedGoogle Scholar
  87. 87.
    Quintana, F. J., and Cohen, I. R. (2004) The natural autoantibody repertoire and autoimmune disease, Biomed. Pharmacother., 58, 276–281.PubMedGoogle Scholar
  88. 88.
    Oka, Y, Hirabayashi, Y, Ikeda, T, Fujii, H., Ishii, T, and Harigae, H. (2011) A single-stranded DNA-cross-reactive immunogenic epitope of human homocysteine-inducible endoplasmic reticulum protein, Scand. J. Immunol., 74, 296–303.PubMedGoogle Scholar
  89. 89.
    Allos, B. M., Lippy, F. T, Carlsen, A., Washburn, R. G., and Blaser, M. J. (1998) Campylobacter jejuni strains from patients with Guillain-Barre syndrome, Emerg. Infect. Dis., 4, 263–268.PubMedCentralPubMedGoogle Scholar
  90. 90.
    Thornton, C. A., and Morgan, G. (2009) Innate and adaptive immune pathways to tolerance, Nestle Nutr. Workshop Ser. Pediatr. Program., 64, 45–57.PubMedGoogle Scholar
  91. 91.
    Janeway, C. A., and Medzhitov, R. (2002) Innate immune recognition, Annu. Rev. Immunol., 20, 197–216.PubMedGoogle Scholar
  92. 92.
    Baldus, S. E., Hanisch, F. G., Kotlarek, G. M., Zirbes, T K., Thiele, J., Isenberg, J., Karsten, U. R., Devine, P. L., and Dienes, H. P. (1998) Coexpression of MUC-1 mucin peptide core and the Thomsen-Friedenreich antigen in colorectal neoplasms, Cancer, 82, 1019–1027.PubMedGoogle Scholar
  93. 93.
    Gorshkova, T. A. (2007) The Plant Cell Wall as a Dynamic System [in Russian], Nauka, Moscow, p. 426.Google Scholar
  94. 94.
    Bovin, N. V. (2013) Natural antibodies to glycans, Biochemistry (Moscow), 78, 786–797.Google Scholar
  95. 95.
    Knirel, Y. A., Gabius, H.-J., Blixt, O., Rapoport, E. M., Khasbiullina, N. R., Shilova, N. V., and Bovin, N. V. (2014) Human tandem-repeat-type galectins bind bacterial non-ßGal polysaccharides, Glycoconj. J., 31, 7–12.PubMedGoogle Scholar
  96. 96.
    Hakomori, S. (2001) The glycosynapse, PNAS, 99, 2252.32.Google Scholar
  97. 97.
    Hakomori, S., and Handa, K. (2015) GM3 and cancer, Glycoconj. J., 32, 1–8.PubMedGoogle Scholar
  98. 98.
    Todeschini, A. R., Dos Santos, J. N., Handa, K., and Hakomori, S. (2008) Ganglioside GM2/GM3 complex affixed on silica nanospheres strongly inhibits cell motility through CD82/cMet-mediated pathway, Proc. Natl. Acad. Sci. USA, 105, 1925–1930.PubMedCentralPubMedGoogle Scholar
  99. 99.
    Di Virgilio, F. (2013) The therapeutic potential of modifying inflammasomes and NOD-like receptors, Pharmacological, 65, 872–905.Google Scholar
  100. 100.
    Mills, K. H. (2011) TLR-dependent T cell activation in autoimmunity, Nature Rev. Immunol., 11, 807–822.Google Scholar
  101. 101.
    Gellert, M. (1997) Recent advances in understanding V(D)J recombination, Adv. Immunol., 64, 39–64.PubMedGoogle Scholar
  102. 102.
    Hennings, L., Artaud, C., Jousheghany, F., Monzavi- Karbassi, B., Pashov, A., and Kieber-Emmons, T (2011) Carbohydrate mimetic peptides augment carbohydratereactive immune responses in the absence of immune pathology, Cancers (Basel), 3, 4151–4169.Google Scholar
  103. 103.
    Avrameas, S., Dighiero, G., Lymberi, P., and Guilbert, B. (1983) Studies on natural antibodies and autoantibodies, Ann. Immunol. (Paris), 134, 103–113.Google Scholar
  104. 104.
    Stahl, D., Lacroix-Desmazes, S., Mouthon, L., Kaveri, S. V., and Kazatchkine, M. D. (2000) Analysis of human selfreactive antibody repertoires by quantitative immunoblotting, J. Immunol. Methods, 240, 1–14.PubMedGoogle Scholar
  105. 105.
    Madi, A., Kenett, D. Y, Bransburg-Zabary, S., Merbl, Y, Quintana, F. J., Boccaletti, S., Tauber, A. I., Cohen, I. R., and Ben-Jacob, E. (2011) Analyses of antigen dependency networks unveil immune system reorganization between birth and adulthood, Chaos, 21, 1–11.Google Scholar
  106. 106.
    Springer, G. F. (1971) Blood-group and Forssman antigenic determinants shared between microbes and mammalian cells, Prog. Allergy, 15, 9–77.PubMedGoogle Scholar
  107. 107.
    Bovin, N., Obukhova, P., Shilova, N., Rapoport, E., Popova, I., Navakouski, M., Unverzagt, C., Vuskovic, M., and Huflejt, M. (2012) Repertoire of human natural antiglycan immunoglobulins. Do we have auto-antibodies? Biochim. Biophys. Acta, 1820, 1373–1382.PubMedGoogle Scholar
  108. 108.
    Obukhova, P., Piskarev, V., Severov, V., Pazynina, G., Tuzikov, A., Navakouski, M., Shilova, N., and Bovin, N. (2011) Profiling of serum antibodies with printed glycan array: room for data misinterpretation, Glycocon. J., 28, 501–505.Google Scholar
  109. 109.
    Tupitsyn, N. N., Udalova, Y. A., Galanina, O. E., Kadagidze, Z. G., Borovkova, N. B., Podolsky, V. V., Shinkarev, S. A., Gadetskaya, N. A., Letyagin, V. P., Obukhova, P. S., Shilova, N. V., Subbotina, A. A., and Bovin, N. V. (2009) Tumor-associated glycan Lewis C in breast cancer, Hematopoiesis Immunol., 2, 45–54.Google Scholar
  110. 110.
    Hakomori, S. (1984) Tumor-associated carbohydrate antigens, Annu. Rev. Immunol., 2, 103–126.PubMedGoogle Scholar
  111. 111.
    Lloyd, K. O. (1991) Humoral immune responses to tumor-associated carbohydrate antigens, Semin. Cancer Biol., 2, 421–431.PubMedGoogle Scholar
  112. 112.
    Livingston, P. O. (1995) Augmenting the immunogenicity of carbohydrate tumor antigens, Semin. Cancer Biol., 2, 357–366.Google Scholar
  113. 113.
    Springer, G. F. (1984) T and Tn, general carcinoma autoantigens, Science, 224, 1198–1206.PubMedGoogle Scholar
  114. 114.
    Huflejt, M. E., Vuskovic, M., Vasiliu, D., Xu, H., Obukhova, P., Shilova, N., Tuzikov, A., Galanina, O., Arun, B., Lu, K., and Bovin, N. V. (2009) Anti-carbohydrate antibodies of normal sera: findings, surprises and challenges, Mol. Immunol., 46, 3037–3049.PubMedGoogle Scholar
  115. 115.
    Jacob, F., Goldstein, D. R., Huflejt, M., Bovin, N., Pochechueva, T, Spengler, M., Caduff, R., Fink, D., and Heinzelmann-Schwarz, V. (2012) Serum antiglycan antibody detection of nonmucinous ovarian cancers by using a printed glycan array, Int. J. Cancer, 130, 1381–1346.Google Scholar
  116. 116.
    Bovin, N. V., and Huflejt, M. E. (2008) Unlimited glycochip, Trends Glycosci. Glycotechnol., 20, 245–258.Google Scholar
  117. 117.
    Cheng, H., Yang, Z., Estabrook, M. M., John, C. M., Jarvis, G. A., McLaughlin, S., and Griffiss, M. (2011) Human lipopolysaccharide IgG that prevents endemic meningococcal disease recognizes an internal lacto- N-neotetraose structure, J. Biol. Chem., 286, 4362–243633.Google Scholar
  118. 118.
    Kurtenkov, O., Miljukhina, L., Smorodin, J., Klaamas, K., Bovin, N., Ellamaa, M., and Chuzmarov, V. (1999) Natural IgM and IgG antibodies to Thomsen- Friedenreich (T) antigen in serum of patients with gastric cancer and blood donors, Acta Oncol., 38, 939–943.PubMedGoogle Scholar
  119. 119.
    Lekakh, I. V., Bovin, N. V., Bezyaeva, G. P., and Poverenny, A. M. (2001) Natural hidden autoantibodies react with negatively charged carbohydrates and xenoantigen Bdi, Biochemistry (Moscow), 66, 205–210.Google Scholar
  120. 120.
    Krenn, V., von Landenberg, P., Wozniak, E., Kissler, C., Hermelink, H. K., Zimmermann, U., and Vollmers, H. P. (1995) Efficient immortalization of rheumatoid synovial tissue B-lymphocytes. A comparison between the techniques of electric field-induced and PEG fusion, Hum. Antibodies Hybridomas, 6, 47–51.PubMedGoogle Scholar
  121. 121.
    Anthony, R. M., and Ravetch, J. V. (2010) A novel role for the IgG Fc glycan: the anti-inflammatory activity of sialylated IgG Fcs, J. Clin. Immunol., 30, 9–14.Google Scholar
  122. 122.
    Stadlmann, J., Pabst, M., and Altmann, F. (2010) Analytical and functional aspects of antibody sialylation, J. Clin. Immunol., 30, 15–19.PubMedCentralGoogle Scholar
  123. 123.
    Wassenaar, T. M., and Panigrahi, P. (2014) Is a fetus developing in a sterile environment? Lett. Appl. Microbiol., 59, 572–579.PubMedGoogle Scholar
  124. 124.
    Aagaard, K. M. (2014) Author response to comment on “the placenta harbors a unique microbiome”, Sci. Transl. Med., 6, 254–256.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2015

Authors and Affiliations

  1. 1.Shemyakin—Ovchinnikov Institute of Bioorganic ChemistryRussian Academy of SciencesMoscowRussia

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