Peptidoglycans as promoters of slow-wave sleep. II. Somnogenic and pyrogenic activities of some naturally occurring muramyl peptides; correlations with mass spectrometric structure determination.
Open accessAbstract
The structures of components of the sleep-promoting material purified from human urine were established by fast atom bombardment-mass spectrometry, as reported in the accompanying paper (Martin, S. A., Karnovsky, M. L., Krueger, J. M., Pappenheimer, J. R., and Biemann, K. (1984) J. Biol. Chem. 259, 12652-12658). We report here that two substances isolated from that preparation, viz. N-acetylglucosaminyl-1,6 -anhydro-N-acetylmuramyl-Ala-gamma-Glu-diaminopimelyl-Ala) and that compound lacking the terminal alanine, are active as somnogens. Cerebro-intraventricular administration of 1 pmol of the glycotetrapeptide was sufficient to induce prolonged excess sleep in rabbits. A similar substance obtained from Brevibacterium divaricatum in which the free carboxyls of the glutamic and diaminopimelic moieties, indicated above, were amidated (N-acetylglucosaminyl-1,6-anhydro-N-anhydromura-myl-Ala-iso- Gln- epsilon-amido-diaminopimelyl -Ala-Ala) was not active as a promoter of slow-wave sleep. Deamidation of this peptide to a mixture of the free dicarboxylic forms produced a somnogenic substance. Our findings show that in addition to the muramyl form of peptidoglycan monomers, the anhydro muramyl form, with no reducing end, is compatible with somnogenic activity. Furthermore, the data obtained with a natural product amplify our earlier observations with smaller synthetic molecules of the importance of amidation/deamidation in the structure-activity relationships of muramyl peptides.
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The first bacterial component demonstrated to alter sleep was a specific muramyl peptide derived from bacterial cell wall peptidoglycans.
“The first bacterial component demonstrated to alter sleep was a specific muramyl peptide derived from bacterial cell wall peptidoglycans (Krueger et al, 1984).”
From Sleep health: Reciprocal regulation of sleep and innate immunity (2017) · cites this paper as Krueger et al, 1984
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Peptidoglycan types of bacterial cell walls and their taxonomic implications
SCHLEIFER, K. H., & Kandler, O. (1972) · Bacteriological Reviews · doi:10.1128/br.36.4.407-477.1972 · Cited by 4,203 · see citing works
Dinarello, C. A. (1984) · Clinical Infectious Diseases · doi:10.1093/clinids/6.1.51 · Cited by 1,647 · see citing works
Fontana, A., Kristensen, F., Dubs, R., Gemsa, D., & Weber, E. (1982) · The Journal of Immunology · doi:10.4049/jimmunol.129.6.2413 · Cited by 752 · see citing works
Pappenheimer, J. R., Koski, G., Fencl, V., Karnovsky, M. L., & Krueger, J. M. (1975) · Journal of Neurophysiology · doi:10.1152/jn.1975.38.6.1299 · Cited by 270 · see citing works
Self-citationHughes, J. R. (1985) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(85)91080-6 · Cited by 247 · see citing works
Sleep-promoting effects of muramyl peptides.
Krueger, J. M., Pappenheimer, J. R., & Karnovsky, M. L. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.19.6102 · Cited by 228 · see citing works
Self-citationThe composition of sleep-promoting factor isolated from human urine.
Krueger, J. M., Pappenheimer, J. R., & Karnovsky, M. L. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)68088-9 · Cited by 192 · see citing works
Self-citationSleep-promoting effects of cerebrospinal fluid from sleep-deprived goats.
Pappenheimer, J. R., Miller, T. B., & Goodrich, C. A. (1967) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.58.2.513 · Cited by 177 · see citing works
Self-citationFactors in cerebrospinal fluid from goats that affect sleep and activity in rats*
Fencl, V., Koski, G., & Pappenheimer, J. R. (1971) · The Journal of Physiology · doi:10.1113/jphysiol.1971.sp009541 · Cited by 128 · see citing works
Self-citationMartin, S. A., Karnovsky, M. L., Krueger, J. M., Pappenheimer, J. R., & BIEMANN, K. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)90795-7 · Cited by 114 · see citing works
Self-citationMuramyl peptides. Variation of somnogenic activity with structure.
Krueger, J. M., Walter, J., Karnovsky, M. L., CHEDID, L. A., Choay, J., Lefrancier, P., & LEDERER, E. (1984) · The Journal of Experimental Medicine · doi:10.1084/jem.159.1.68 · Cited by 98 · see citing works
Self-citationQualitative detection of muramic acid in normal mammalian tissues
Sen, Z., & Karnovsky, M. L. (1984) · Infection and Immunity · doi:10.1128/iai.43.3.937-941.1984 · Cited by 57 · see citing works
Self-citationSleep-promoting factor S: purification and properties.
Krueger, J. M., Pappenheimer, J. R., & Karnovsky, M. L. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.10.5235 · Cited by 46 · see citing works
Self-citationYapo, A., Petit, J. F., LEDERER, E., Parant, M., Parant, F., & CHEDID, L. A. (1982) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(82)90042-x · Cited by 24 · see citing works
Immunomodulation by muramyl peptides: Recent developments
LEDERER, E. (1982) · Clinical Immunology Newsletter · doi:10.1016/s0197-1859(82)80059-9 · Cited by 18 · see citing works
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Clarke, T. B., Davis, K. M., Lysenko, E. S., Zhou, A. Y., Yu, Y., & Weiser, J. N. (2010) · Nature Medicine · doi:10.1038/nm.2087 · Cited by 1,154 · see citing works
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Puga, I., Cols, M., Barra, C., He, B., Cassis, L., Gentile, M., Comerma, L., Chorny, A., Shan, M., Xu, W., et al. (2011) · Nature Immunology · doi:10.1038/ni.2194 · Cited by 731 · see citing works
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Irwin, M. R., & Opp, M. R. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.148 · Cited by 624 · see citing works
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Matenchuk, B. A., Mandhane, P. J., & Kozyrskyj, A. L. (2020) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2020.101340 · Cited by 495 · see citing works
Opp, M. R. (2005) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2005.01.002 · Cited by 393 · see citing works
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Krueger, J. M. (2003) · Frontiers in Bioscience · doi:10.2741/1033 · Cited by 329 · see citing works
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Arentsen, T., Qian, Y., Gkotzis, S., Femenia, T., Wang, T., Udekwu, K., Forssberg, H., & Diaz Heijtz, R. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.182 · Cited by 280 · see citing works
Hobson, J. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00371.1990 · Cited by 247 · see citing works
Lytic transglycosylases: concinnity in concision of the bacterial cell wall
Dik, D. A., Marous, D. R., Fisher, J. F., & Mobashery, S. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1337705 · Cited by 164 · see citing works
Alteration of sleep in rabbits by Staphylococcus aureus infection
Toth, L. A., & Krueger, J. M. (1988) · Infection and Immunity · doi:10.1128/iai.56.7.1785-1791.1988 · Cited by 159 · see citing works
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Correia, J. D. S., Miranda, Y., Austin-Brown, N., Hsu, J. C., Mathison, J. C., Xiang, R., Zhou, H., Li, Q., Han, J., & Ulevitch, R. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509228103 · Cited by 121 · see citing works
Krueger, J. M., & Opp, M. R. (2016) · International Review of Neurobiology · doi:10.1016/bs.irn.2016.07.003 · Cited by 120 · see citing works
Self-citationInvited review: MDP and other muropeptides — direct and synergistic effects on the immune system
Traub, S., von Aulock, S., Härtung, T., & Hermann, C. (2006) · Journal of Endotoxin Research · doi:10.1179/096805106x89044 · Cited by 115 · see citing works
Martin, S. A., Karnovsky, M. L., Krueger, J. M., Pappenheimer, J. R., & BIEMANN, K. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)90795-7 · Cited by 114 · see citing works
Self-citationPrimary structure of the peptidoglycan-derived tracheal cytotoxin of Bordetella pertussis
Cookson, B. T., Tyler, A. N., & Goldman, W. E. (1989) · Biochemistry · doi:10.1021/bi00430a048 · Cited by 110 · see citing works
Krueger, J. M., Takahashi, S., Kapás, L., Bredow, S., Roky, R., Fang, J., Floyd, R. A., Renegar, K. B., Guha‐Thakurta, N., Novitsky, S. V., et al. (1995) · Advances in Neuroimmunology · doi:10.1016/0960-5428(95)00007-o · Cited by 98 · see citing works
Self-citationDelta-sleep-inducing peptide (DSIP): An update
Graf, M., & Kastin, A. J. (1986) · Peptides · doi:10.1016/0196-9781(86)90148-8 · Cited by 98 · see citing works
Sleep, neuroimmune and neuroendocrine functions in fibromyalgia and chronic fatigue syndrome
Moldofsky, H. (1995) · Advances in Neuroimmunology · doi:10.1016/0960-5428(94)00048-s · Cited by 95 · see citing works
Microbiota signalling through MyD88 is necessary for a systemic neutrophilic inflammatory response
Karmarkar, D., & Rock, K. L. (2013) · Immunology · doi:10.1111/imm.12159 · Cited by 89 · see citing works
Fleming, T. J., Wallsmith, D. E., & Rosenthal, R. S. (1986) · Infection and Immunity · doi:10.1128/iai.52.2.600-608.1986 · Cited by 85 · see citing works
Peptidoglycan sensing by octopaminergic neurons modulates Drosophila oviposition
Kurz, C. L., Charroux, B., Chaduli, D., Viallat-Lieutaud, A., & Royet, J. (2017) · eLife · doi:10.7554/elife.21937 · Cited by 78 · see citing works
Engel, H., Kazemier, B., & Keck, W. (1991) · Journal of Bacteriology · doi:10.1128/jb.173.21.6773-6782.1991 · Cited by 75 · see citing works
The biology of bacterial peptidoglycans and their impact on host immunity and physiology
Wheeler, R., Chevalier, G., Eberl, G., & Boneca, I. G. (2014) · Cellular Microbiology · doi:10.1111/cmi.12304 · Cited by 69 · see citing works
Dokter, W. H. A., Dijkstra, A. J., Koopmans, S., Stulp, B. K., Keck, W., Halie, M. R., & Vellenga, E. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)41763-7 · Cited by 65 · see citing works
Sleep as a host defense: Its regulation by microbial products and cytokines
Krueger, J. M., & Majde, J. A. (1990) · Clinical Immunology and Immunopathology · doi:10.1016/0090-1229(90)90033-m · Cited by 65 · see citing works
Self-citationSensory neuron–associated macrophages as novel modulators of neuropathic pain
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Hesek, D., Lee, M., Zhang, W., Noll, B. C., & Mobashery, S. (2009) · Journal of the American Chemical Society · doi:10.1021/ja808498m · Cited by 64 · see citing works
Human immune system during sleep.
Asif, N., Iqbal, R., & Chaudhry, F. N. (2017) · PubMed Central · Cited by 64 · see citing works
Neuroscience-driven discovery and development of sleep therapeutics
Dresler, M., Spoormaker, V. I., Beitinger, P., Czisch, M., Kimura, M., Steiger, A., & Holsboer, F. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.10.012 · Cited by 63 · see citing works
Neuroendocrine immune interactions in health and disease
Masˇek, K., Slánský, J., Petrovický, P., & Hadden, J. W. (2003) · International Immunopharmacology · doi:10.1016/s1567-5769(03)00015-8 · Cited by 63 · see citing works
Role of Glia in the Regulation of Sleep in Health and Disease
Garofalo, S., Picard, K., Limatola, C., Nadjar, A., Pascual, O., & Tremblay, M. (2020) · Comprehensive physiology · doi:10.1002/cphy.c190022 · Cited by 63 · see citing works
Krueger, J. M., Majde, J. A., & Obál, F. (2003) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(02)00065-x · Cited by 61 · see citing works
Self-citationKrueger, J. M., & Karnovsky, M. L. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb35808.x · Cited by 59 · see citing works
Self-citationEffects of Muramyl Peptides on Macrophages, Monokines, and Sleep
Pabst, M. J., Beranová-Giorgianni, Š., & Krueger, J. M. (1999) · NeuroImmunoModulation · doi:10.1159/000026384 · Cited by 58 · see citing works
Self-citationRehman, A., Taishi, P., Fang, J., Majde, J. A., & Krueger, J. M. (2001) · Cytokine · doi:10.1006/cyto.2000.0800 · Cited by 55 · see citing works
Self-citationA conserved domain in putative bacterial and bacteriophage transglycosylases
Koonin, E. V., & Rudd, K. E. (1994) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(94)90201-1 · Cited by 54 · see citing works
Martin, S. A., Rosenthal, R. S., & BIEMANN, K. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47596-5 · Cited by 53 · see citing works
Self-citationMolinaro, R., Mukherjee, T., Flick, R., Philpott, D. J., & Girardin, S. E. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.007997 · Cited by 49 · see citing works
Murein-metabolizing enzymes from Escherichia coli: existence of a second lytic transglycosylase
Engel, H., Smink, A. J., van Wijngaarden, L., & Keck, W. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.20.6394-6403.1992 · Cited by 45 · see citing works
Structure and immunochemistry of meningococcal lipopolysaccharides
Jennings, H. J., Beurret, M., Gamian, A., & Michon, F. (1987) · Antonie van Leeuwenhoek · doi:10.1007/bf00415511 · Cited by 45 · see citing works
Biological properties of bacterial peptidoglycan
Johannsen, L. (1993) · Apmis · doi:10.1111/j.1699-0463.1993.tb00119.x · Cited by 44 · see citing works
The NOD2 signaling in peripheral macrophages contributes to neuropathic pain development
Santa-Cecília, F. V., Ferreira, D. W., Guimarães, R. M., Cecílio, N. T., Fonseca, M. M., Lopes, A. H., Davoli-Ferreira, M., Kusuda, R., de Souza, G. R., Nachbur, U., et al. (2018) · Pain · doi:10.1097/j.pain.0000000000001383 · Cited by 42 · see citing works
Leung, A. K.-W., Duewel, H. S., Honek, J. F., & Berghuis, A. M. (2001) · Biochemistry · doi:10.1021/bi0028035 · Cited by 41 · see citing works
Bausteine von Oligosacchariden, LXIX. Synthese von 1,6‐Anhydromuramylpeptiden
Paulsen, H. M., Himpkamp, P., & Peters, T. (1986) · Liebigs Annalen der Chemie · doi:10.1002/jlac.198619860408 · Cited by 41 · see citing works
Meltzer, L. T., Serpa, K. A., & Moos, W. H. (1989) · Psychopharmacology · doi:10.1007/bf00634462 · Cited by 41 · see citing works
Kelland, J. G., Arnold, L. D., Palcic, M. M., Pickard, M. A., & Vederas, J. C. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)69293-2 · Cited by 39 · see citing works
Cardinali, D. P., Pagano, E. S., Bernasconi, P. A. S., Reynoso, R., & Scacchi, P. A. (2011) · PubMed · Cited by 38 · see citing works
Root-Bernstein, R. S., & Westall, F. C. (1990) · Brain Research Bulletin · doi:10.1016/0361-9230(90)90178-3 · Cited by 37 · see citing works
Krueger, J. M., Rosenthal, R. S., Martin, S. A., Walter, J., Davenne, D., Shoham, S., Kubillus, S. L., & BIEMANN, K. (1987) · Brain Research · doi:10.1016/0006-8993(87)90062-x · Cited by 35 · see citing works
Self-citationParant, M., Pouillart, P., Contel, C. L., Parant, F., CHEDID, L. A., & Bahr, G. M. (1995) · Infection and Immunity · doi:10.1128/iai.63.1.110-115.1995 · Cited by 34 · see citing works
Krueger, J. M., Davenne, D., Walter, J., Shoham, S., Kubillus, S. L., Rosenthal, R. S., Martin, S. A., & BIEMANN, K. (1987) · Brain Research · doi:10.1016/0006-8993(87)90063-1 · Cited by 32 · see citing works
Self-citationActivation of B cells by non‐canonical helper signals
Cerutti, A., Cols, M., & Puga, I. (2012) · EMBO Reports · doi:10.1038/embor.2012.111 · Cited by 29 · see citing works
Sleep as a neuroimmune phenomenon: A brief historical perspective
Krueger, J. M., & Karnovsky, M. L. (1995) · Advances in Neuroimmunology · doi:10.1016/0960-5428(94)00047-r · Cited by 29 · see citing works
Self-citationSomnogenic activity of O-acetylated and dimeric muramyl peptides
Johannsen, L., Rosenthal, R. S., Martin, S. A., Cady, A. B., Obál, F., Guinand, M., & Krueger, J. M. (1989) · Infection and Immunity · doi:10.1128/iai.57.9.2726-2732.1989 · Cited by 28 · see citing works
Self-citationProperties of the Cell Surfaces of Pathogenic Bacteria
Doyle, R. J., & Sonnenfeld, E. M. (1989) · International review of cytology · doi:10.1016/s0074-7696(08)60872-4 · Cited by 25 · see citing works
Peptidoglycan fragments decrease food intake and body weight gain in rats
Biberstine, K. J., & Rosenthal, R. S. (1994) · Infection and Immunity · doi:10.1128/iai.62.8.3276-3281.1994 · Cited by 24 · see citing works
Recent developments in the field of biologically active peptides
Schmidt, G. (1986) · Topics in current chemistry · doi:10.1007/3-540-16724-2_8 · Cited by 23 · see citing works
Dokter, W. H. A., Dijkstra, A. J., Koopmans, S., Mulder, A., Stulp, B. K., Halie, M. R., Keck, W., & Vellenga, E. (1994) · Infection and Immunity · doi:10.1128/iai.62.7.2953-2957.1994 · Cited by 20 · see citing works
Recent Advances in the Synthesis and Biological Applications of Peptidoglycan Fragments
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Somnogenic activity of muramyl peptides
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Self-citationHabjanec, L., Halassy, B., & Tomašić, J. (2010) · International Immunopharmacology · doi:10.1016/j.intimp.2010.04.005 · Cited by 18 · see citing works
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Opp, M. R., & Krueger, J. M. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-24288-2.00019-2 · Cited by 18 · see citing works
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Cabeza, R. D. J., Zoltoski, R. K., & Gillin, J. C. (1994) · Elsevier eBooks · doi:10.1016/b978-0-7506-9002-7.50009-4 · Cited by 18 · see citing works
Moldofsky, H., Martin, J., James, K., Walter, C., Dinarello, A., Lue, F. A., Quance, G., & Oreopoulos, D. G. (1985) · Peritoneal Dialysis International · doi:10.1177/089686088500500314 · Cited by 16 · see citing works
Serotonergic aspects of the response of human platelets to immune-adjuvant muramyl dipeptide
Polanski, M., & Karnovsky, M. L. (1992) · Journal of Neuroimmunology · doi:10.1016/0165-5728(92)90166-i · Cited by 16 · see citing works
Self-citationHuang, C.-L., Chu, H.-F., Wu, C.-C., Deng, F.-S., Wen, P.-J., Chien, S.-P., Chao, C., Chen, Y.-T., Lu, M., & Tsai, Y.-C. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1209067 · Cited by 15 · see citing works
Root-Bernstein, R. S. (2015) · Anti-Cancer Agents in Medicinal Chemistry · doi:10.2174/1871520615666150716105057 · Cited by 15 · see citing works
Cardinali, D. P., & Esquifino, A. I. (2012) · Current Immunology Reviews · doi:10.2174/157339512798991263 · Cited by 15 · see citing works
Optimization of sample deposition for plasma‐desorption mass spectrometry of peptidoglycan monomers
Allmair, G., Caparrós, M., & Pittenauer, E. (1992) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.1290060412 · Cited by 15 · see citing works
Feng, M., Gao, B., Garcia, L. R., & Sun, Q. H. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1035582 · Cited by 13 · see citing works
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Chatterjee, B., Mondal, D., & Bera, S. (2021) · Tetrahedron · doi:10.1016/j.tet.2021.132403 · Cited by 13 · see citing works
Engel, H., van Leeuwen, A., Dijkstra, A. J., & Keck, W. (1992) · Applied Microbiology and Biotechnology · doi:10.1007/bf00174845 · Cited by 13 · see citing works
Somnogenic activity of muramyl peptide-derived immune adjuvants
Johannsen, L., Orál, F., Kapás, L., Kovalzon, V. M., & Krueger, J. M. (1994) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(94)90066-3 · Cited by 13 · see citing works
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Polanski, M., Vermeulen, M. W., Wu, J., & Karnovsky, M. L. (1995) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(94)00097-8 · Cited by 12 · see citing works
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Root-Bernstein, R. S., & Dillon, P. F. (2008) · Current Pharmaceutical Design · doi:10.2174/138161208783330727 · Cited by 12 · see citing works
Crystallization of the soluble lytic transglycosylase from Escherichia coli K12
Rozeboom, H. J., Dijkstra, B. W., Engel, H., & Keck, W. (1990) · Journal of Molecular Biology · doi:10.1016/0022-2836(90)90221-7 · Cited by 12 · see citing works
Past, present and future of psychoneuroimmunology
Mašek, K. (2000) · Toxicology · doi:10.1016/s0300-483x(99)00143-2 · Cited by 12 · see citing works
Post-Myocardial Infarction Depression
Rousseau, G., Bah, T. M., & Godbout, R. (2012) · InTech eBooks · doi:10.5772/33408 · Cited by 10 · see citing works
Roten, C.-A. H., & Karamata, D. (1992) · Cellular and Molecular Life Sciences · doi:10.1007/bf01919139 · Cited by 8 · see citing works
Endogenous hypometabolic-hypothermic factors and their possible application to life in the cold
Kramarova, L. I., Ziganshin, R., & Gakhova, E. N. (2009) · Russian Journal of Bioorganic Chemistry · doi:10.1134/s1068162009050021 · Cited by 7 · see citing works
Krueger, J. M., Opp, M. R., Toth, L. A., Johannsen, L., & Kapás, L. (1990) · Current topics in neuroendocrinology · doi:10.1007/978-3-642-75837-9_10 · Cited by 7 · see citing works
Self-citationCytokine Involvement in Sleep Responses to Infection and Physiological Sleep
Krueger, J. M. (1996) · Neuroscience intelligence unit · doi:10.1007/978-1-4615-9695-0_4 · Cited by 6 · see citing works
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Polanski, M., JOHNSON, T. S., & Karnovsky, M. L. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb49125.x · Cited by 5 · see citing works
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Silverman, D. H. S., & Karnovsky, M. L. (1989) · Advances in enzymology and related areas of molecular biology/Advances in enzymology and related subjects · doi:10.1002/9780470123089.ch5 · Cited by 5 · see citing works
Self-citationKimura, M., Honda, K., Komoda, Y., & Inoué, S. (1987) · Neuroscience Research · doi:10.1016/0168-0102(87)90031-9 · Cited by 5 · see citing works
Krueger, J. M., & Majde, J. A. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-6645-3.00025-6 · Cited by 4 · see citing works
Self-citationBaquero, F., Ayala, J. A., & Cantón, R. (2026) · Microbial Drug Resistance · doi:10.1177/10766294261431312 · Cited by 3 · see citing works
Pharmacology of the CNS Peptides
Inoue, S. (1995) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-57836-6_9 · Cited by 3 · see citing works
From Natural Products Chemistry to Immunopharmacology
LEDERER, E. (1986) · Elsevier eBooks · doi:10.1016/b978-0-08-032008-3.50004-7 · Cited by 3 · see citing works
Role of biological membranes in slow-wave sleep
Karnovsky, M. L. (1991) · Journal of Bioenergetics and Biomembranes · doi:10.1007/bf00768842 · Cited by 3 · see citing works
Self-citationMechanisms linking sleep, innate immunity, and neuroinflammation
Opp, M. R., Rowe, R. K., & Krueger, J. M. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106803 · Cited by 2 · see citing works
Self-citationLocal and niche-adapted sleep regulatory mechanisms encompass the holobiont condition
English, E. L., & Krueger, J. M. (2025) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2025.102145 · Cited by 2 · see citing works
Self-citationRosenthal, R. S., & Krueger, J. M. (1987) · Antonie van Leeuwenhoek · doi:10.1007/bf00415512 · Cited by 2 · see citing works
Self-citationImmune-neuroendocrine-thermal mechanisms and the sleep-wake system.
Moldofsky, H. (1994) · American Psychological Association eBooks · doi:10.1037/10166-003 · Cited by 2 · see citing works
Krueger, J. M., & Majde, J. A. (2005) · Elsevier eBooks · doi:10.1016/b0-72-160797-7/50028-8 · Cited by 2 · see citing works
Self-citationHumoral and Other Sleep-Promoting Factors
Szentirmai, É., & Kapás, L. (2021) · Springer eBooks · doi:10.1007/978-3-030-65574-7_11 · Cited by 1 · see citing works
Endogenous factors controlling sleep
Pollard, B. J., Haywood, P. B., & Pomfrett, C. J. D. (2002) · Current Anaesthesia and Critical Care · doi:10.1054/cacc.2002.0377
- Authors
- Krueger, J. M., Karnovsky, M. L., Martin, S. A., Pappenheimer, J. R., Walter, J., & Biemann, K.
- Affiliations
- Massachusetts Institute of Technology (US)
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 1984-10
- Volume
- 259
- Issue
- 20
- Pages
- 12659-12662
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W1588673077
- Cited by
- 111
- References
- 15
- Citations by year
- 2026: 3 · 2025: 1 · 2023: 2 · 2022: 1 · 2021: 3 · 2020: 4 · 2019: 1 · 2018: 1 · 2017: 4 · 2016: 4 · 2015: 1 · 2014: 1 · 2013: 3 · 2012: 4
- FWCI
- 4.27
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Keywords
- peptidoglycan, slow-wave sleep, muramyl peptides, pyrogenicity, structure-activity relationship, deamidation, amidation, human urine
- MeSH terms
- Acetylmuramyl-Alanyl-Isoglutamine, Animals, Biological Assay, Body Temperature, Cerebral Ventricles, Glycopeptides, Humans, Male, Peptidoglycan, Rabbits, Sleep Stages, Mass Spectrometry, Structure-Activity Relationship
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