Immunomodulating and Related Biological Activities of Bacterial Cell Walls and Their Components, Enzymatically Prepared or Synthesized

  • Shozo Kotani
  • Haruhiko Takada
  • Masachika Tsujimoto
  • Tomohiko Ogawa
  • Keijiro Kato
  • Takafumi Okunaga
  • Yoshitaka Ishihara
  • Akinori Kawasaki
  • Ichijiro Morisaki
  • Nagayuki Kono
  • Tsutomu Shimono
  • Tetsuo Shiba
  • Shoichi Kusumoto
  • Masaru Inage
  • Kazuhiro Harada
  • Toshiyuki Kitaura
  • Seisaburo Kano
  • Shinya Inai
  • Kazuyoshi Nagai
  • Misako Matsumoto
  • Takashi Kubo
  • Masahiko Kato
  • Zenichi Tada
  • Kanae Yokogawa
  • Shigeo Kawata
  • Atsuo Inoue

Abstract

In 1959, we isolated the cell walls of tubercle bacilli (BCG) which have long been known to have a strong immunoadjuvant activity, especially in the stimulation of cell-mediated immune responses, and elucidated the chemical and immunological properties of this cell wall fraction (32, 31). The most remarkable finding on the chemical composition of this subcellular fraction was that various lipids, especially ethanol-ether insoluble but chloroform-soluble lipids and bound lipids, which characterized tubercle bacilli were almost exclusively localized in their cell walls. It was also demonstrated that the cell walls were the most active fraction of subcellular components isolated from sonicated BCG cells, in inducing tuberculin hypersensitivity in guinea pigs and that the cell walls were involved in the development of an acquired cell-mediated resistance of mice to tuberculous infection.

Keywords

Cholesterol Influenza Bacillus Malaria Lysozyme 

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References

  1. 1.
    Adam, A., Ellouz, F., Ciorbaru, R., Petit, J. F., and Lederer, E., 1975, Peptidoglycan adjuvants: minimal structure required for activity. Z. Immun.-Forsch. 149(s): 341,Google Scholar
  2. 2.
    Appleyard, G., and Maber, H. B., 1974, Plaque formation by influenza viruses in the presence of trypsin. J. Gen. Virol. 25: 351.PubMedCrossRefGoogle Scholar
  3. 3.
    Audibert, F., Chedid, L., and Hannoun, C., 1977, Augmentation de la response immunitaire au vaccin grippal par un glycopeptide synthetique adjuvant (N-acetylmuramly-L-alanyl-D-isoglutamine), C. R. Acad. Sc. Paris, Serie D. 285: 467.Google Scholar
  4. 4.
    Azuma, I., Kishimoto, S., Yamamura, Y., and Petit, J. F., 1971, Adjuvanticity of mycobacterial cell walls. Jpn. J. Microbiol. 15: 193.PubMedGoogle Scholar
  5. 5.
    Azuma, I., Sugimura, K., Taniyama, T., Yamawaki, M., Yamamura, Y., Kusumoto, S., Okada, S., and Hiba, T., 1976, Adjuvant activity of mycobacterial fractions: adjuvant activity of synthetic N-acetylmuramyl-dipeptide and the related compounds. Infect. Immun. 14: 18.Google Scholar
  6. 6.
    Azuma, I., Sugimura, K, Yamamura, Y., Kusumoto, S., Tarumi, Y, and Shiba, T., 1976, Adjuvant activity of synthetic cjell wall peptidoglycan subunits on onoazobenzenearsonate-N-aceytl-L- tyrosine and bacterial a-amylase in guinea pigs. Jpn. J. Microbiol. 2: 63.Google Scholar
  7. 7.
    Azuma, I., Sugimura, K., Yamawaki, M., Uemiya, M., Kusumoto, S., Okada, S., Shiba, T., and Yamamura, Y., 1978, Adjuvant activity of synthetic 6-l,mycoloyl,,-N-acetylmuramyl-L-alanyl-D-isogluta- mine and related compounds. Infect. ImmuriT 20: 6007Google Scholar
  8. 8.
    Azuma, I., Sugimura, K., Yamawaki, M., Uemiya, M., and Yamamura, Y., 1977, Mitogenic activity of cell-wall components in mouse spleen cells. Microbiol. Immunol. 21: 111.PubMedGoogle Scholar
  9. 9.
    Chedid, L., 1978, Past, present and future of the synthetic immunoadjuvant MDP and its analogs. Biochem. Pharmacol. 27: 2183.Google Scholar
  10. 10.
    Chedid, L., 1979, Immunostimulation. Springer Semin. Immuno- pathol. 2: 1.Google Scholar
  11. 11.
    Chedid, L., Audibert, F., and Johnson, A. G., 1978, Biological activities of muramyl dipeptide, a synthetic glycopeptide analogous to bacterial immunoregulating agents. Prog. Allergy. 25: 63.PubMedGoogle Scholar
  12. 12.
    Chedid, L., Audibert, F., and Parant, M., 1978, Une nouvelle famille limmunoregulateurs synthetiques: le muramyl dipeptide et ses analogues. Path. Biol. 26: 527.Google Scholar
  13. 13.
    Ellouz, F., Adam, A., Ciorbaru, R., and Lederer, E., 1974, Minimum structural requirements for adjuvant activity of bacterial peptidoglycan derivatives. Biochem. Biophys. Res. Commun. 59: 1317.PubMedCrossRefGoogle Scholar
  14. 14.
    Emori, K., and Tanaka, A., 1978, Granuloma formation by synthetic bacterial cell wall fragment: Muramyl dipeptide. Infect. Immun. 19: 613.PubMedGoogle Scholar
  15. 15.
    Hamada, S., Narita, T., Kotani, S., and Kato, K., 1971, Studies on cell, walls of group A Streptococcus pyogenes, type 12. II. Pyrogenic and related biological activities of the higher molecular weight fraction of an enzymatic digest of the cell walls. Biken J. 14: 217.PubMedGoogle Scholar
  16. 16.
    Heymer, B., 1975, Biological properties of the peptidoglycan, Z. Immun.-Forsch. 149 (S): 245.Google Scholar
  17. 17.
    Heymer, B., Finger, H., and Wirsing, C.-H., 1978, Immunoadjuvant effects of the synthetic muramyl-dipeptide (MDP) N-acetylmuramyl- L-alanyl-D-isoglutamine. Z. Immun.-Forsch. 155: 87.Google Scholar
  18. 18.
    Igarashi, T., Okada, M., Azuma, I, and Yamamura, Y., 1977, Adjuvant activity of synthetic N-acetylmuramyl-L-alanyl-D- isoglutamine and related compounds on cell-mediated cytotoxicity in syngeneic mice. Cell. Immunol. 34: 270.PubMedCrossRefGoogle Scholar
  19. 19.
    Inai, S., Nagai, K., Ebisu, S., Kato, K., Kotani, S., and Misaki, A., 1976, Activation of the alternative complement pathway by water-insoluble glycans of Streptococcus mutans: The relation between their chemical structures and activating potencies. Immunol. 117: 1256.Google Scholar
  20. 20.
    Koga, T., Maeda, K., Onoue, K., Kato, K., and Kotani, S., 1979, Chemical structure required for immunoadjuvant and arthrito- genic activities of cell wall peptidoglycans. Mol. Immunol. 16: 153.PubMedCrossRefGoogle Scholar
  21. 21.
    Koga, T., Pearson, C. M., Narita, T., and Kotani, S., 1973, Polyarthritis induced in the rat with cell walls from several bacteria and two Streptomyces sp. Proc. Soc. Exp. Biol. Med. 143: 824.Google Scholar
  22. 22.
    Koga, T., Kotani, S., Narita, T., and Pearson, C. M., 1976, Induction of adjuvant arthritis in the rat by various bacterial cell walls and their water-soluble components. Int. Arch. Allergy Appl. Immun. 51: 206.Google Scholar
  23. 23.
    Kohashi, O., Pearson, C. M., Beck, F. W. J., Narita, T., and Kotani, S., 1976, Arthritogenicity in rats of cell walls from several streptococci, Staphylococci and two other bacteria. Proc. Soc. Exp. Biol. Med. 152: 199.Google Scholar
  24. 24.
    Kohashi, O., Pearson, C. M., Shimono, T., and Kotani, S., 1976, Preparation of various fractions from Mycobacterium smegmatis, their arthritogenicity and their preventive effect on adjuvant disease. Int. Arch. Allergy Appl. Immun. 51: 451.CrossRefGoogle Scholar
  25. 25.
    Kohashi, O., Pearson, C. M., Watanabe, Y., Kotqni, S., and Koga, T., 1976, Structural requirements for arthritogenicity of peptidoglycans from Staphylococcus aureus and Lactobacillus plantarum and analogous synthetic compounds. J. Immun. 116: 1635.PubMedGoogle Scholar
  26. 26.
    Kotani, S., Harada, K., Kitaura, T., Hashimoto, Y., Matsubara, T., and Chimori, M., 1962, Lysis of isolated BCG cell walls with enzymes. Biken J. 5: 117.PubMedGoogle Scholar
  27. 27.
    Kotani, S., Hashimoto, S., Matsubara, T., Kato, K., Harada, K., Kogami, J., Kitaura, T., and Tanaka, A., 1963, Lysis of isolated BCG cell walls with enzymes II. Demonstration of bound wax DT as a component of BCG cell walls. Biken J. 6: 181.Google Scholar
  28. 28.
    Kotani, S., Kinoshita, F., Morisaki, I., Shimono, T., Okunaga, T., Takada, H., Tsuijimoto, M., Watanabe, Y., Kato, K., Shiba, T., Kusumoto, S., and Okada, S., 1977, Immunoadjuvant activities of synthetic 6-0-acyl-N-acetylmuramyl-L-alanyl-D-isoglutamine with special reference to the effect oT its administration with liposomes. Biken J. 20: 95.PubMedGoogle Scholar
  29. 29.
    Kotani, S., Kinoshita, F., Watanabe, Y., Morisaki, I., Shimono, T., Kato, K., Shiba, T., Kusumoto, S., Ikenaka, K., and Tarumi, Y., 1977, Effects of chemical modification of the glutamic acid residue in N-acetylmuramyl peptides on the immunoadjuvancies of the molecules. Biken J. 20: 125.Google Scholar
  30. 30.
    Kotani, S., Kitaura, T., Hashimoto, S., Chimori, M., and Kishida, H., 1964. Influence of extraction of bound wax Df of BCG with trichloroacetic acid on its adjuvant activity on development of a delayed type of hypersensitivity. Biken J. 6: 321.PubMedGoogle Scholar
  31. 31.
    Kotani, S., Kitaura, T., Higashigawa, M., Kato, K., Mori, Y., Matsubara, T., and Tsujimoto, T., 1960, Studies on the immunological properties of the cell wall-, particle- and soluble- fractions of sonicated BCG cells. Biken J. 3: 159.Google Scholar
  32. 32.
    Kotani, S., Kitaura, T., Hirano, T., and Tanaka, A., 1959, Preparation and chemical composition of the cell walls of BCG. Biken J. 2: 129.Google Scholar
  33. 33.
    Kotani, S., Matsubara, T., Kitaura, T., Mori, Y., Chimori, M., and Kishida, H., 1963, Adjuvant activity in development of a delayed type of hypersensitivity of a lipid fraction isolated from enzymatically digested cell walls of Corynebacterium diphtheriae. Biken J. 6: 211.PubMedGoogle Scholar
  34. 34.
    Kotani, S., Narita, T., Stewart-Tull, D. E. S., Shimono, T., Watanabe, Y., Kato, K., and Iwata, S., 1975, Immunoadjuvant activities of cell walls and their water-soluble fractions prepared from various gram-positive bacteria. Biken J. 18: 77.PubMedGoogle Scholar
  35. 35.
    Kotani, S., Watanabe, Y., Kinoshita, F., Kato, K., Harada, K., Shiba, T., Kusumoto, S., Tarumi, Y., Idenaka, K., and Okada, S., 1977, Gelation of the amoebocyte lysate of Tachypleus tridentatusby cell wall digest of several gram-positive bacterial and synthetic peptidoglycan subunits of natural and unnatural configurations. Biken J. 20: 5.PubMedGoogle Scholar
  36. 36.
    Kotani, S., Watanabe, Y., Kinoshita, F., Kato, K., and Perkins, H. R., 1977, Immunoadjuvant activities of the enzymatic digests of bacterial cell walls lacking immunoadjuvancy by themselves. Biken J. 20: 87.PubMedGoogle Scholar
  37. 37.
    Kotani, S., Watanabe, Y., Kinoshita, F., Kato, K., Schleifer, K. H., Perkins, H. R., 1977, Inabilities as an immunoadjuvant of cell walls of the group B peptidoglycan types and those of arthrobacters. Biken J. 20: 1.PubMedGoogle Scholar
  38. 38.
    Kotani, S., Watanabe, Y., Kinoshita, F., Morisake, I., Kato, K., Shiba, T., Kusumoto, S., Tarumi, Y., and Ikenaka, K., 1977, The effect of replacement of L-alanine residue by glycine, L- serine or D-alanine in an N-ac etylmuramy 1-L-alany 1-D-isogluTfa- mine on immunoadjuvancies of molecules. Biken J. 20: 39.Google Scholar
  39. 39.
    Kotani, S., Watanabe, Y., Kinoshita, F., Shimono, T., Morisaki, I., Shiba, T., Kusumoto, S., Tarumi, Y., and Idenaka, K., 1975, Immunoadjuvant activities of synthetic N-acetylmuramy1-peptides of -amino acids. Biken J. 18: 105.PubMedGoogle Scholar
  40. 40.
    Kotani, S., Watanabe, Y., Narita, T., Shimono, T., Stewart-Tull, D.E.S., Iwata, S., Yamaguchi, H., Iwata, K., Shimizu, T., Mifuchi, I., Nozawa, Y., Ito, Y., Kanetsuna, F., Yano, K., Misaki, A., Matsuoka, T., and Fukui, K., 1975, Immunoadjuvant activities of fungal cell walls. Biken J. 18: 135.PubMedGoogle Scholar
  41. 41.
    Kotani, S., Watanabe, Y., Shimono, T., Harada, K., Shiba, T., Kusumoto, S., Yokogawa, K., and Taniguchi, M., 1976, Correlation between the immunoadjuvant activities and pyrogenicities of synthetic N-acetylmuramly-peptides and -amino acids. Biken J. 19: 9.PubMedGoogle Scholar
  42. 42.
    Kotani, S., Watanabe, Y., Shimono, T., Kinoshita, F., Narita, T., Kato, K., Stewart-Tull, D. E. S., Morisaki, I., Yokogawa, K., and Kawata, S., 1975, Immunoadjuvant activities of peptidoglycan subunits from the cell walls of Staphylococcus aureus and Lactobacillus plantarum. Biken J. 18: 83.Google Scholar
  43. 43.
    Kotani, S., Watanabe, Y., Shimono, T., Narita, T., Kato, K., Stewart-Tull, D. E. S., Kinoshita, F., Yokogawa, K., Kawata, S., Shiba, T., Kusumoto, S., and Tarumi, Y., 1975, Immunoadjuvant activities of cell walls, their water-soluble fractions and peptidoglycan subunits, prepared from various gram-positive bacteria, and of synthetic N-acetylmuramy1 peptides. Z. Immun. -Forsch. 149 (S): 302.Google Scholar
  44. 44.
    Krause, R. M., 1975, Immunological activity of the peptidoglycan. Z. Immun. -Forsch. 149 (S): 136.Google Scholar
  45. 45.
    Kusumoto, S., Inage, M., and Shiba, T., 1978, Synthesis of long chain fatty acid esters of N-acetylmuramyl-L-alanyl-D-iso- glutamine in relation to antitumor activity? Tetrahedron Lett. 49: 4899.CrossRefGoogle Scholar
  46. 46.
    Kusumoto, S., Okada, S., Yamamoto, K., and Shiba, T., 1978, Synthesis of 6-0-acyl derivatives of immunoadjuvant active N-acetylmuramy1-L-alany1-D-isoglutamine. Bull. Chem. Soc. Jpn. 51: 2122.Google Scholar
  47. 47.
    Kusumoto, S., Tarumi, Y., Ikenaka, K., Shiba, T., 1976, Chemical synthesis of N-acetylmuramyl peptides with partial structures of bacterial cell wall and their analogs in relation to immuno- adjuvant activities. Bull. Chem. Soc. Jpn. 49: 533.Google Scholar
  48. 48.
    Masek, K., Zaoral, M., Jezek, J., and Strake, R., 1978, Immuno- adjuvant activity of synthetic N-acetylmuramyl dipeptide. Experientia 34: 1363.PubMedCrossRefGoogle Scholar
  49. 49.
    Midtvedt, T., and Melby, K., 1978, Phagocytosis of 32P-labelled E. coli by human polymorphonuclear cells (PMN). Acta Path. Microbiol. Scand. Sect. B. 86: 193.Google Scholar
  50. 50.
    Nagai, Y., Akiyama, K., Kotani, S., Watanabe, Y., Shimono, T., Shiba, T., and Kusumoto, S., 1978, Structural specificity of synthetic peptide adjuvant for induction of experimental allergic encephalomyelitis, Cell. Immunol. 35: 168.Google Scholar
  51. 51.
    Nagai, Y., Akiyama, K., Suzuki, K., Kotani, S., Watanabe, Y., Shimono, T., Shiba, T., Kusumoto, S., Ikuta, F., and Takeda, S., 1978, Minimum structural requirements for encephalitogen and for adjuvant in the induction of experimental allergic encepha-lomyelitis. Cell. Immunol. 35: 158.Google Scholar
  52. 52.
    Nagao, S., Tanaka, A., Yamamoto, Y., Koga, T., Onoue, K., Shiba, T., Kusumoto, S., and Kotani, S., 1979, Inhibition of macrophage migration by muramyl peptides. Infect. Immun. 24: 308.Google Scholar
  53. 53.
    Narita, T., Hamada, S., Kotani, S., Hasegawa, K., and Ishida, T., 1971, Studies on cell walls of group A Streptococcus pyogenes, type 12. III. Cardiac lesions produced in mice by a higher molecular weight fraction isolated from a digest of cell walls, with the L-ll enzyme. Biken J. 14: 233.Google Scholar
  54. 54.
    Ohkuni, H., Norose, Y., Hayama, M., Kimura, Y., Kotani, S., Shiba, T., Kusumoto, S., Yokogawa, K., and Kawata, S., 1977, Adjuvant activities in production of reaginic antibody in mice of bacterial cell wall peptidoglycans or peptidoglycan subunits and of synthetic N-acetylmuramyl-dipeptides. Biken J. 20: 131.PubMedGoogle Scholar
  55. 55.
    Ohkuni, H., Norose, Y., Ohta, M., Hayama, M., Tsujimoto, M., Kotani, S., Shiba, T., Kusumoto, S., Yokogawa, K., and Kawata, S., 1979, Adjuvant activities in production of reaginic antibody by bacterial cell wall peptidoglycan or synthetic N-acetyl- muramyl dipeptides in mice. Infect. Immun. 24: 313.Google Scholar
  56. 56.
    Parant, M., 1979, Biological properties of a new synthetic adjuvant, muramyl dipeptide (MDP). Springer Semin. Immunopathol. 2: 101.Google Scholar
  57. 57.
    Raskova, H., Rye, M., Rotta, J., and Masek, K., 1971, Release of 5-hydroxy-tryptamine and morphological changes in blood platelets induced by mucopeptide of streptococcal cell walls. J. Infec. Pis. 123: 587.CrossRefGoogle Scholar
  58. 58.
    Rotta, J., 1975, Endotoxin-like properties of the peptidoglycan. Z. Immun.-Forsch. 149 (S): 230.Google Scholar
  59. 59.
    Rotta, J., Rye, M., Masfek, K., and Azoral, M.,1979, Biological activity of synthetic subunits of streptococcus peptidoglycan. I. Pyrogenic and thrombocytolytic activity. Expt. Cell. Biol. 47: 257.Google Scholar
  60. 60.
    Rye, M., and Rotta, J., 1975, The thrombocytolytic activity of bacterial peptidoglycan. Z. Immun.-Forsch. 149 (S): 265–272.Google Scholar
  61. 61.
    Schleifer, K. H., and Kandler, O., 1972, Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36: 407.Google Scholar
  62. 62.
    Schleifer, K. H., and Seidel, P. H., 1974, The immunochemistry of peptidoglycan. Antibodies against a synthetic immunogen crossreacting with peptidoglycan. Eur. J. Biochem. 43: 509.Google Scholar
  63. 63.
    Schwab, J. H., and Smialowicz, R., 1975, Interaction of bacterial cell wall polymers and rat macrophages. Z. Immun.-Forsch. 149 (S): 283.Google Scholar
  64. 64.
    Seidel, P. H., and Schleifer, K. H., 1977, The immunochemistry of peptidoglycan. Antibodies against a synthetic immunogen crossreacting with an interpeptide bridge of peptidoglycan. Eur. J. Biochem. 74: 353.Google Scholar
  65. 65.
    Shiba, T., Okada, S., Kusumoto, S., Azuma, I., and Yamamura, Y., 1978, Synthesis of 6-0-mycoloyl-N=acetylmuramyl-L-alanyl- D-isoglutamine with antitumor activity. Bull. Chem. Soc. Jpn. 51: 3307.Google Scholar
  66. 66.
    Siddiqui, W. A., Taylor, D. W., Kan, S.-C., Kramer, K., Richmond-Crum, S.M., Kotani, S., Shiba, T., and Kusumoto, S.. 1978, Vaccination of experimental monkeys against Plasmodium falciparum: A possible safe adjuvant. Science. 201: 1237.Google Scholar
  67. 67.
    Smith, S. M., Burrel, R., and Snyder, I. S., 1978, Complement activation by cell wall fractions of Miczopolyspora faeni. Infect. Immun. 22: 568.Google Scholar
  68. 68.
    Snyder, S. H., Axelrod, J., and Zweig, M., 1965, A sensitive and specific fluorescence assay for tissue serotonin. Biochem Pharmacol. 14: 831.PubMedCrossRefGoogle Scholar
  69. 69.
    Stewart-Tull, D. E. S., Shimono, T., Kotani, S., Kato, M., Ogawa, Y., Yamamura, Y., Koga, T., and Pearson, C. M., 1975, The adjuvant activity of a non-toxic water-soluble glycopeptide present in large quantities in the culture filtrate of Mycobacterium tuberculosis strain DT. Immunology 29: 1.PubMedGoogle Scholar
  70. 70.
    Stewart-Tull, D. E. S., Shimono, T., Kotani, S., and Knights, B. K., 1976, Immunosuppressive effect in mycobacterial adjuvant emulsions of mineral oils containing low molecular weight hydrocarbons. Int. Arch. Allergy Appl. Immun. 52: 118.Google Scholar
  71. 71.
    Sugimura, K., Uemiya, M., Saiki, I., Azuma, I., and Yamamura, Y., 1979, The adjuvant activity of synthetic N-acetylmuramly-di- peptide: Evidence of initial target cells for the adjuvant activity. Cell. Immunol. 43: 137.Google Scholar
  72. 72.
    Takada, H., Kotani, S., Kusumoto, S.,Tarumi, Y., Ikenaka, K., and Shiba,T., 1977, Mitogenic activity of adjuvant-active N- acetylmuramyl-L-alanyl-D-isoglutamine and its analogues. Biken J. 20: 81.PubMedGoogle Scholar
  73. 73.
    Takada, H., Tsugimoto, M., Kato, K., Kotani, S., Kusumoto, S., Inage, M., Shiba, T., Yano, I., Kawata, S., and Yokogawa, K., 1979, Macrophage activation by bacterial cell walls and related synthetic compounds. Infect. Immun. 25: 48.PubMedGoogle Scholar
  74. 74.
    Takada, H., Tsujimoto, M., Kotani, S., Kusumoto, S., Inage, M., Shiba, T., Nagao, S., Yano, I., Kawata, S., and Yokogawa, K., 1979, Mitogenic effects of bacterial cell walls, their fragments, and related synthetic compounds on thymocytes and splenocytes of guinea pigs. Infect. Immun. 25: 645.PubMedGoogle Scholar
  75. 75.
    Tanaka, A., Nagao, S., Nagao(Saito), R., Kotani, S., Kusumoto, S., and Shiba, T., 1979, Stimulation of the reticuloendothelial system of mice by muramyl dipeptide. Infect. Immun. 24: 302.Google Scholar
  76. 76.
    Tanaka, A., Nagao, S., Saito, R., Kotani, S., Kusumoto, S., and Shiba, T., 1977, Correlation of stereochemically specific structure in muramyl dipeptide between macrophage activation and adjuvant activity. Biochem. Biophys. Res. Commun. 77: 621.Google Scholar
  77. 77.
    Tanaka, A., Saito, R., Sugiyama, S., Morisaki, I., Kotani, S., Kusumoto, S., and Shiba, T., 1977, Adjuvant activity of syn-thetic N-acetlnpujramyi peptides in rats. Infect. Immun. 15: 332.Google Scholar
  78. 78.
    Trippestad, A., and Midtvedt, T., 1968, Phagocytosis of 32P- labelled IS. coli by rat peritoneal polymorphonuclear leukocytes. Evaluation of a method. Acta Path. Microbiol. Scand. 74: 259.Google Scholar
  79. 79.
    Tsujimoto, M., Kinoshita, F., Okunaga, T., Kotani, S., Kusumoto, S., Yamamoto, K., and Sljiba, T., 1979, Higher immunoadjuvant activities of N-acetyl-3-D-glutaminyl-(l-4)-N-acetylmuramyl-L -alanyl-D-isoglutamine in comparison with N-acetylmuramyl-L-— alanyl-D-isoglutamine. Microbiol. Immunol. 23: 933.Google Scholar
  80. 80.
    Uemiya, M., Saiki, I., Kusama, T., Azuma, I., and Yamamura, Y., 1979, Adjuvant activity of mycoloyl derivatives of N-acetyl- muramyl-L-alanyl-D-isoglutamine in mice and guinea pigs. Micro-biol. Immunol. 23T 821.Google Scholar
  81. 81.
    Uemiya, M., Sugimura, K., Kusama, T., Saiki, I., Yamawaki, M., Azuma, I., and Yamamura, Y., 1979, Adjuvant activity of 6-0- mycoloyl derivatives of N-acetylmuramyl-L-seryl-D-isoglutamine and related compounds in mice and guinea pigs. Tnfect. Immun. 24: 83.Google Scholar
  82. 82.
    Wahl, S. M., Wahl, L. M., McCarthy, B., Chedid, L., and Mergenhagen, S. E., 1979, Macrophage activation by mycobacterial water soluble compounds and synthetic muramyl dipeptide. J. Immunol. 122: 2226.PubMedGoogle Scholar
  83. 83.
    Webster, R. G., Glezen, W. P., Hannoun, G., and Laver, W. G., 1977, Potentiation of the immune response to influenza virus subunit vaccines. J. Immunol. 119: 2073.Google Scholar
  84. 84.
    Wildfener, A., Heymer, B., Spliker, D., Schleifer, K. H., Vanek, E., and Haferkamp, O., 1975, Use of Limulus assay to compare the biological activity of peptidoglycan and endotoxin. Z. Immun.-Forsch. 149 (S): 258.Google Scholar
  85. 85.
    Yamamoto, Y., Nagao, S., Tanaka, A., Koga, T., and Onoue, K., 1978, Inhibition of macrophage migration by synthetic muramyl dipeptide. Biochem. Biophys. Res. Commun. 80: 923.Google Scholar
  86. 86.
    Yamamura, Y., Azuma, I., Sugimura, K., Kusumoto, S., and Shiba, T., 1976, Immunological activity of synthetic cell-wall peptidoglycan subunits. Proc. Jpn. Acad. 52: 58.Google Scholar
  87. 87.
    Yamamura, Y., Azuma, I., Sugimura, K., Yamawakim, M., Uemiya, M., Kusumoto, S., Okada, S., and Shiba, T., 1976, Adjuvant activity of 6-0-mycoloyl-N-acetylmuramyl-L-alanyl-D-isoglutamine Gann 67: 867.Google Scholar
  88. 88.
    Yamamura, Y., Azuma, I., Sugimura, K., Yamawaki, M., Uemiya, M., Kusumoto, S., Okada, S., and Shiba, T., 1977, Immunological and antitumor activities of synthetic 60-mycoloyl-N-acetylmuramyl- dipeptides. Proc. Jpn. Acad. 53: 63.Google Scholar
  89. 89.
    Yamamura, Y., Azuma, I., Taniyama, T., Sugimura, K., Hirao, F., Tokuzen, R., Okabe, M., Nakahara, W., Yasumoto, K., and Ohta, M., 1977, Immunotherapy of cancer with cell wall skeleton of Mycobacterium bovis-Bacillus Calmette-Guerin: Experimental and clinical results. Ann. N.Y. Acad. Sci. 277: 209.Google Scholar
  90. 90.
    Yokogawa, K., Kawata, S., Takemura, T., and Yoshimura, Y., 1975, Purification and properties of lytic enzymes from Streptomyces globisporus 1829. Agr. Biol. Chem. 29: 1533.Google Scholar

Copyright information

© Plenum Press, New York 1981

Authors and Affiliations

  • Shozo Kotani
    • 1
  • Haruhiko Takada
    • 1
  • Masachika Tsujimoto
    • 1
  • Tomohiko Ogawa
    • 1
  • Keijiro Kato
    • 1
  • Takafumi Okunaga
    • 2
  • Yoshitaka Ishihara
    • 2
  • Akinori Kawasaki
    • 3
  • Ichijiro Morisaki
    • 4
  • Nagayuki Kono
    • 4
  • Tsutomu Shimono
    • 4
  • Tetsuo Shiba
    • 5
  • Shoichi Kusumoto
    • 5
  • Masaru Inage
    • 5
  • Kazuhiro Harada
    • 6
  • Toshiyuki Kitaura
    • 6
  • Seisaburo Kano
    • 7
  • Shinya Inai
    • 8
  • Kazuyoshi Nagai
    • 8
  • Misako Matsumoto
    • 8
  • Takashi Kubo
    • 9
  • Masahiko Kato
    • 9
  • Zenichi Tada
    • 9
  • Kanae Yokogawa
    • 10
  • Shigeo Kawata
    • 10
  • Atsuo Inoue
    • 11
  1. 1.Department of Microbiology and Oral MicrobiologyOsaka University Dental SchoolKita-ku, Osaka, 530Japan
  2. 2.The 2nd Department of Oral SurgeryOsaka University Dental SchoolKita-ku, Osaka, 530Japan
  3. 3.The 1st Department of Prosthetic DentistryOsaka University Dental SchoolKita-ku, Osaka, 530Japan
  4. 4.Department of PedodonticsOsaka University Dental SchoolKita-ku, Osaka, 530Japan
  5. 5.Faculty of ScienceOsaka UniversityToyonaka, Osaka, 560Japan
  6. 6.Laboratory of MicrobiologyOsaka Prefectural Institute for Public HealthHigashinari-ku, Osaka, 537Japan
  7. 7.Department of Pharmacology and BacteriologyNational Institute of Hygienic SciencesHigashi-ku, Osaka, 541Japan
  8. 8.Division of ImmunologyThe Center for Adult DiseaseHigashi-ku, Osaka, 537Japan
  9. 9.Kanonji Institute, The Research Foundation for Microbial DiseasesOsaka UniversityKanonji, Kagawa, 768Japan
  10. 10.Research and Development DivisionDainippon Pharmaceutical Co.Suita, Osaka, 564Japan
  11. 11.New Product Planning DepartmentDaiichi Seyaku Co.Chuo-ku, Tokyo, 103Japan

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