Microbiome-induced Antimicrobial Peptides: The Host-defense Weapon Unravelling Drug Designing

Tushar Kanta Garnaik; Santwana Palai; Kautuk Kumar Sardar; Subash Chandra Parija; Tapas Kumar Goswami

doi:10.5455/ijlr.20201109063433

Authors

Tushar Kanta Garnaik MVSc Scholar, Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Odisha University of Agriculture & Technology (OUAT), Bhubaneswar, Odisha, INDIA
Santwana Palai Assistant Professor, Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Odisha University of Agriculture & Technology (OUAT), Bhubaneswar, Odisha, INDIA
Kautuk Kumar Sardar Professor, Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Odisha University of Agriculture & Technology (OUAT), Bhubaneswar, Odisha, INDIA
Subash Chandra Parija Professor & Head, Department of Veterinary Pharmacology and Toxicology, College of Veterinary Science and Animal Husbandry, Odisha University of Agriculture & Technology (OUAT), Bhubaneswar, Odisha, INDIA
Tapas Kumar Goswami Former Principal Scientist, Division of Immunology, ICAR-Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh, INDIA

DOI:

https://doi.org/10.5455/ijlr.20201109063433

Keywords:

AMPs, Defensin, Microbiome, Paneth Cell

Abstract

The present review discusses about the contribution of microbiome that secrete antimicrobial peptides in association with residing microflora of the host imparting antimicrobial activity against invading pathogens. The relationship between antimicrobial peptides and microbiota of the intestine and their resultant effects on host health are highlighted. Defensins, cathelicidins, brevinins, ranalexin etc. can be harnessed as potential therapeutic targets for diseases like ileal Crohns disease, inflammatory bowel disease, colon cancer, etc. The bottom line is to make use of the antimicrobial peptides over the years to scientifically respond to infective agents in terms of therapeutic options in the treatment of animal diseases.

References

Allaire, J. M., Crowley, S. M., Law, H. T., Chang, S. Y., Ko, H. J., & Vallance, B. A. (2018). The intestinal epithelium: central coordinator of mucosal immunity. Trends in Immunology, 39(9), 677-696. DOI:10.1016/j.it.2018.04

Berg, R. D. (1996). The indigenous gastrointestinal microflora. Trends in Microbiology, 4(11), 430-435. DOI:10.1016/0966-842x (96)10057-3

Blaser, M. J. (2006). Who are we? Indigenous microbes and the ecology of human diseases. EMBO Reports, 7(10), 956-960. DOI:10.1038/sj.embor.7400812

Boman, HG., Nilsson, I., Rasmuson, B. (1972) Inducible antibacterial defence system in drosophila. Nature, 237 (5352):232–235. DOI:10.1038/237232a0

Bourlioux, P., Koletzko, B., Guarner, F., & Braesco, V. (2003). The intestine and its microflora are partners for the protection of the host: report on the Danone Symposium “The Intelligent Intestine,” held in Paris, June 14, 2002. The American Journal of Clinical Nutrition, 78(4), 675-683. DOI: 10.1093/ajcn/78.4.675

Cazorla, S. I., Maldonado-Galdeano, C., Weill, R., De Paula, J. and Perdigon, G.D.V. (2018). Oral Administration of probiotics increases paneth cells and intestinal antimicrobial activity. Frontiers in Microbiology, 9:736; DOI: 10.3389 /fmicb.2018.00736

Cinar, K., Diler, A., & Bilgin, F. (2001). Immunohistochemical localization of some peptides in the gastrointestinal tract mucosa of pike-perch (Stizostedion lucioperca L., 1758). Turkish Journal of Veterinary and Animal Sciences, 25(3), 369-375.

Cobo, E. R., & Chadee, K. (2013). Antimicrobial human β-defensins in the colon and their role in infectious and non-infectious diseases. Pathogens, 2(1), 177-192. DOI:10.3390/pathogens2010177

Cuthbert, A. P., Fisher, S. A., Mirza, M. M., King, K., Hampe, J., Croucher, P. J. & Schreiber, S. (2002). The contribution of NOD2 gene mutations to the risk and site of disease in inflammatory bowel disease. Gastroenterology, 122(4), 867-874. DOI:10.1053/gast.2002.32415

Da Costa, J. P., Cova, M., Ferreira, R., & Vitorino, R. (2015). Antimicrobial peptides: an alternative for innovative medicines? Applied Microbiology and Biotechnology, 99(5), 2023-2040. DOI:10.1007/s00253-015-6375-x

Diamond, G., Beckloff, N., Weinberg, A., & Kisich, K. O. (2009). The roles of antimicrobial peptides in innate host defense. Current Pharmaceutical Design, 15(21), 2377-2392. DOI: 10.2174/138161209788682325

Dominguez-Bello, M. G., Blaser, M. J., Ley, R. E., & Knight, R. (2011). Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology, 140(6), 1713-1719. DOI:10.1053/j.gastro.2011.02.011

Duquesne, S., Petit, V., Peduzzi, J., & Rebuffat, S. (2007). Structural and functional diversity of microcins, gene-encoded antibacterial peptides from enterobacteria. Journal of Molecular Microbiology and Biotechnology, 13(4), 200-209. DOI:10.1159/000104748

Dutta, P., & Das, S. (2016). Mammalian antimicrobial peptides: promising therapeutic targets against infection and chronic inflammation. Current Topics in Medicinal Chemistry, 16(1), 99-129. DOI: 10.2174/1568026615666150703121819

Fellermann, K., Wehkamp, J., Herrlinger, K. R., & Stange, E. F. (2003). Crohn's disease: a defensin deficiency syndrome? European Journal of Gastroenterology & Hepatology, 15(6), 627-634. DOI: 10.1097/01.meg.0000059151.68845.88

Fons, Ana Gomez, Tuomo Karjalainen, M. (2000). Mechanisms of colonisation and colonisation resistance of the digestive tract part 2: bacteria/bacteria interactions. Microbial Ecology in Health and Disease, 12(2), 240-246. DOI:10.1080/089106000750060495

Gill, S. R., Pop, M., DeBoy, R. T., Eckburg, P. B., Turnbaugh, P. J., Samuel, B. S., ... & Nelson, K. E. (2006). Metagenomic analysis of the human distal gut microbiome. Science, 312(5778), 1355-1359. DOI: 10.1126/science.1124234

Gordon, Y. J., Romanowski, E. G., & McDermott, A. M. (2005). A review of antimicrobial peptides and their therapeutic potential as anti-infective drugs. Current Eye Research, 30(7), 505-515. DOI: 10.1080/02713680590968637

Goswami T and Kumar S. 2011. Antimicrobial peptide: An ancient goal keeper playing at center forward in defense game. Emerging Science, III, 10–16.

Gurao, A., Kataria, R., Kashyap, S., & Singh, R. (2018). Sequence Characterization and Insilico Anti-biofilm Activity Prediction of beta Defensin 103A in Tharparkar Cattle Breed and Taurine Cattle. International Journal of Livestock Research, 8(10), 365-381. DOI: 10.5455/ijlr.20180226061317

Han, V. K. M., Sayed, H., Chance, G. W., Brabyn, D. G., & Shaheed, W. A. (1983). An outbreak of Clostridium difficile necrotizing enterocolitis: a case for oral vancomycin therapy? Pediatrics, 71(6), 935-941. DOI :PMID: 6856405

Hancock, R. E. (2001). Cationic peptides: effectors in innate immunity and novel antimicrobials. The Lancet Infectious Diseases, 1(3), 156-164. DOI:10.1016/S1473-3099(01)00092-5

Hancock, R. E., & Sahl, H. G. (2006). Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nature Biotechnology, 24(12), 1551-1557. DOI :10.1038/nbt1267

Harwig, S. S., Waring, A., Yang, H. J., Cho, Y., Tan, L., & Lehrer, R. I. (1996). Intramolecular disulfide bonds enhance the antimicrobial and lytic activities of protegrins at physiological sodium chloride concentrations. European Journal of Biochemistry, 240(2), 352-357. DOI: 10.1111/j.1432-1033.1996.0352h.x.

Hassan, M., Kjos, M., Nes, I. F., Diep, D. B., & Lotfipour, F. (2012). Natural antimicrobial peptides from bacteria: characteristics and potential applications to fight against antibiotic resistance. Journal of Applied Microbiology, 113(4), 723-736. DOI:10.1111/j.1365-2672.2012.05338.x

Ho, P., & Ross, D. A. (2017). More than a gut feeling: the implications of the gut microbiota in psychiatry. Biological Psychiatry, 81(5), e35-e37. DOI: 10.1016/j.biopsych.2016.12.018

Hristova, K., Selsted, M. E., & White, S. H. (1997). Critical role of lipid composition in membrane permeabilization by rabbit neutrophil defensins. Journal of Biological Chemistry, 272(39), 24224-24233. DOI:10.1074/jbc.272.39.24224

Hultmark, D., Steiner, H., Rasmuson, T., & Boman, H. G. (1980). Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. European Journal of Biochemistry, 106(1), 7-16. DOI: :10.1111/j.1432-1033.1980.tb05991.x

Ivanov, I. I., & Honda, K. (2012). Intestinal commensal microbes as immune modulators. Cell Host & Microbe, 12(4), 496-508. DOI:10.1016/j.chom.2012.09.009

Jager, S., Stange, E. F., & Wehkamp, J. (2010). Antimicrobial peptides in gastrointestinal inflammation. International Journal of Inflammation, 2010. 1-11. DOI:10.4061/2010/910283

Janeway, C. A., Travers, P., Walport, M., & Capra, J. D. (1999). The complement system in humoral immunity. Immunobiology: The Immune System in Health and Disease, 339-359. ISBN 0-8153-3217-3

Johnson, K. V. A. (2020). Gut microbiome composition and diversity are related to human personality traits. Human Microbiome Journal, 15, 100069. DOI: 10.1016/j.humic.2019.100069

Koenig, J. E., Spor, A., Scalfone, N., Fricker, A. D., Stombaugh, J., Knight, R., ... & Ley, R. E. (2011). Succession of microbial consortia in the developing infant gut microbiome. Proceedings of the National Academy of Sciences, 108(Supplement 1), 4578-4585. DOI: 10.1073/pnas.1000081107

Kopp, Z. A., Jain, U., Van Limbergen, J., & Stadnyk, A. W. (2015). Do antimicrobial peptides and complement collaborate in the intestinal mucosa? Frontiers in Immunology, 6, 17. DOI:10.3389/fimmu.2015.00017

Kruis, W., Fric, P., & Stolte, M. S. (2001). Maintenance of remission in ulcerative colitis is equally effective with Escherichia coli Nissle 1917 and with standard mesalamine. Gastroenterology, 120(5), A127. DOI:10.1016/S0016-5085(08)80625-7

Kubler, I., Koslowski, M. J., Gersemann, M., Fellermann, K., Beisner, J., Becker, S., ... & Wehkamp, J. (2009). Influence of standard treatment on ileal and colonic antimicrobial defensin expression in active Crohn’s disease. Alimentary Pharmacology & Therapeutics, 30(6), 621-633. DOI :10.1111/j.1365-2036.2009.04070.x

Lencer, W. I., Cheung, G., Strohmeier, G. R., Currie, M. G., Ouellette, A. J., Selsted, M. E., & Madara, J. L. (1997). Induction of epithelial chloride secretion by channel-forming cryptdins 2 and 3. Proceedings of the National Academy of Sciences, 94(16), 8585-8589. DOI:10.1073/pnas.94.16.8585

Liévin-Le Moal, V., & Servin, A. L. (2006). The front line of enteric host defense against unwelcome intrusion of harmful microorganisms: mucins, antimicrobial peptides, and microbiota. Clinical Microbiology Reviews, 19(2), 315-337. DOI: 10.1128/CMR.19.2.315-337.2006

Martínez, B., Rodríguez, A., & Suárez, E. (2016). Antimicrobial peptides produced by bacteria: the bacteriocins. In New weapons to control bacterial growth (pp. 15-38). Springer, Cham. (2): 15-38. DOI:10.1007/978-3-319-28368-5

Mason, D. Y., & Taylor, C. R. (1975). The distribution of muramidase (lysozyme) in human tissues. Journal of Clinical Pathology, 28(2), 124-132. DOI: 10.1136/jcp.28.2.124

Mi, Gujie, et al. "Self‐assembled arginine‐rich peptides as effective antimicrobial agents." Journal of Biomedical Materials Research Part A 105.4 (2017): 1046-1054. DOI: 10.1002/jbm.a.35979

Mo, Y., Lorenzo, M., Farghaly, S., Kaur, K., & Housman, S. T. (2019). What's new in the treatment of multidrug-resistant gram-negative infections? Diagnostic Microbiology and Infectious Disease, 93(2), 171-181. DOI: 10.1016/j.diagmicrobio.2018.08.007

Mor, A., & Nicolas, P. (1994). Isolation and structure of novel defensive peptides from frog skin. European Journal of Biochemistry, 219 (1‐2), 145-154. DOI :10.1046/

Mukherjee, S., & Hooper, L. V. (2015). Antimicrobial defense of the intestine. Immunity, 42(1), 28-39. DOI:10.1016/j.immuni.2014.12.028

Mulani, M. S., Kamble, E. E., Kumkar, S. N., Tawre, M. S., & Pardesi, K. R. (2019). Emerging strategies to combat ESKAPE pathogens in the era of antimicrobial resistance: a review. Frontiers in Microbiology, 10, 539. DOI: 10.3389/fmicb.2019.00539

Mulder, I. E., Schmidt, B., Stokes, C. R., Lewis, M., Bailey, M., Aminov, R. I. & Musk, C. C. (2009). Environmentally-acquired bacteria influence microbial diversity and natural innate immune responses at gut surfaces. BMC Biology, 7(1), 79. DOI: 10.1186/1741-7007-7-79

Nguyen, L. T., Haney, E. F., & Vogel, H. J. (2011). The expanding scope of antimicrobial peptide structures and their modes of action. Trends in Biotechnology, 29(9), 464-472. DOI: 10.1016/j.tibtech.2011.05.001

Nguyen, T. X., Cole, A. M., & Lehrer, R. I. (2003). Evolution of primate θ-defensins: a serpentine path to a sweet tooth. Peptides, 24(11), 1647-1654. DOI: 10.1016/j.peptides.2003.07.023

Ouellette, A. J., Hsieh, M. M., Nosek, M. T., Cano-Gauci, D. F., Huttner, K. M., Buick, R. N., & Selsted, M. E. (1994). Mouse Paneth cell defensins: primary structures and antibacterial activities of numerous cryptdin isoforms. Infection and Immunity, 62(11), 5040-5047. DOI: 10.1128/IAI.62.11.5040-5047.1994

Pasupuleti, M., Schmidtchen, A., & Malmsten, M. (2012). Antimicrobial peptides: key components of the innate immune system. Critical Reviews in Biotechnology, 32(2), 143-171. DOI: 10.3109/07388551.2011.594423

Peccia, J., & Kwan, S. E. (2016). Buildings, beneficial microbes, and health. Trends in Microbiology, 24(8), 595-597. DOI: 10.1016/j.tim.2016.04.007

Poirel, L., Madec, J. Y., Lupo, A., Schink, A. K., Kieffer, N., Nordmann, P., & Schwarz, S. (2018). Antimicrobial resistance in Escherichia coli. Antimicrobial Resistance in Bacteria from Livestock and Companion Animals, 289-316. DOI:10.1128/ microbiolspec. ARBA-0026-2017

Porter, E. M., Bevins, C. L., Ghosh, D., & Ganz, T. (2002). The multifaceted Paneth cells. Cellular and Molecular Life Sciences CMLS, 59(1), 156-170. DOI:10.1007/s00018-002-8412-z

Pruthviraj, D. R., Venkatachalapathy, R. T., Usha, A. P., Pramod, S., Pragathi, K. S., & Karthikeyan, A. (2018). Comparative Expression Analysis of Porcine Beta-Defensin-1 Gene between Large White Yorkshire and Ankamali Pigs. International Journal of Livestock Research, 8(4), 71-80. DOI : 10.5455/ijlr.20171113013154

Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., & Mende, D. R. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464(7285), 59-65. DOI:10.1038/nature08821

Rabanal, F., & Cajal, Y. (2016). Therapeutic potential of antimicrobial peptides. In New Weapons to Control Bacterial Growth (pp. 433-451). Springer, Cham.

Rahnamaeian, M. (2011). Antimicrobial peptides: modes of mechanism, modulation of defense responses. Plant Signaling & Behavior, 6(9), 1325-1332. DOI:10.4161/psb.6.9.16319

Rewatkar, H., Wankhede, S., Agashe, J., Padole, R., Jadhao, A., & Jadhao, G. (2019). The Effect of Supplementation of Oregano Oil and Probiotic on Intestinal Microbes (E. coli spp., Salmonella spp., Clostridia spp.) of the Broiler Chicken. International Journal of Livestock Research, 9(7), 77-84. Doi: 10.5455/ijlr.20190504063600

Russell, J. P., Diamond, G., Tarver, A. P., Scanlin, T. F., & Bevins, C. L. (1996). Coordinate induction of two antibiotic genes in tracheal epithelial cells exposed to the inflammatory mediators lipopolysaccharide and tumor necrosis factor alpha. Infection and Immunity, 64(5), 1565-1568. DOI: 10.1128/IAI.64.5.1565-1568.1996

Sanz, J. A., & El Aidy, S. (2019). Microbiota and gut neuropeptides: a dual action of antimicrobial activity and neuroimmune response. Psychopharmacology, 236(5), 1597-1609. DOI : 10.1007/s00213-019-05224-0

Sassone-Corsi, M., Nuccio, S. P., Liu, H., Hernandez, D., Vu, C. T., Takahashi, A. A., ... & Raffatellu, M. (2016). Microcins mediate competition among Enterobacteriaceae in the inflamed gut. Nature, 540(7632), 280-283. DOI:10.1038/nature20557

Sato, H., & Feix, J. B. (2006). Peptide–membrane interactions and mechanisms of membrane destruction by amphipathic α-helical antimicrobial peptides. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1758 (9), 1245-1256. DOI:10.1016/j.bbamem.2006.02.021

Schroeder, B. O., Ehmann, D., Precht, J. C., Castillo, P. A., Küchler, R., Berger, J., & Wehkamp, J. (2015). Paneth cell α-defensin 6 (HD-6) is an antimicrobial peptide. Mucosal Immunology, 8(3), 661-671. DOI: 10.1038/mi.2014.100

Sivieri, K., Bassan, J., Peixoto, G., & Monti, R. (2017). Gut microbiota and antimicrobial peptides. Current Opinion in Food Science, 13, 56-62. DOI :10.1016/j.cofs.2017.02.010

Sharif, N., Sreedevi, B., Chaitanya, R., & Sreenivasulu, D. (2017). Isolation and Identification of the Gut Microbiota of Healthy and Diarrheic Dogs in Andhra Pradesh, India. International Journal of Livestock Research, 7(11), 126-131. DOI : 10.5455/ijlr.20170812034416

Tang, Y. Q., Yuan, J., Ösapay, G., Ösapay, K., Tran, D., Miller, C. J., ... & Selsted, M. E. (1999). A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated α-defensins. Science, 286(5439), 498-502. DOI: 10.1126/science.286.5439.498

Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M., Knight, R., & Gordon, J. I. (2007). The human microbiome project. Nature, 449(7164), 804-810. DOI:10.1038/nature06244

Turner, J. R. (2009). Intestinal mucosal barrier function in health and disease. Nature Reviews Immunology, 9(11), 799-809. DOI:10.1038/nri2653

van t Hof, W., Veerman, E. C., Helmerhorst, E. J., & Amerongen, A. V. N. (2001). Antimicrobial peptides: properties and applicability. Biological Chemistry, 382(4), 597-619. DOI:10.1515/BC.2001.072

Walker, W. A. (2000). Role of nutrients and bacterial colonization in the development of intestinal host defense. Journal of Pediatric Gastroenterology and Nutrition, 30, S2-S7. DOI: 10.1097/00005176-200000002-00002

Walsh, C. T., & Wencewicz, T. A. (2014). Prospects for new antibiotics: a molecule-centered perspective. The Journal of Antibiotics, 67(1), 7-22. DOI: 10.1038/ja.2013.49.

Wu, M., & Hancock, R. E. (1999). Improved derivatives of bactenecin, a cyclic dodecameric antimicrobial cationic peptide. Antimicrobial Agents and Chemotherapy, 43(5), 1274-1276. DOI: 10.1128/AAC.43.5.1274

Xhindoli, D., Pacor, S., Benincasa, M., Scocchi, M., Gennaro, R., & Tossi, A. (2016). The human cathelicidin LL-37—A pore-forming antibacterial peptide and host-cell modulator. Biochimica Et Biophysica Acta (BBA)-Biomembranes, 1858(3), 546-566. DOI:10.1016/j.bbamem.2015.11.003

Zaiou, M., & Gallo, R. L. (2002). Cathelicidins, essential gene-encoded mammalian antibiotics. Journal of Molecular Medicine, 80(9), 549-561. DOI :10.1007/s00109-002-0350-6

Zanetti, M. (2004). Cathelicidins, multifunctional peptides of the innate immunity. Journal of Leukocyte Biology, 75(1), 39-48. DOI: 10.1189/jlb.0403147

Zanetti, M. (2005). The role of cathelicidins in the innate host defenses of mammals. Current Issues in Molecular Biology, 7(2), 179-196. DOI: 10.21775/cimb.007.179

Zanetti, M., Gennaro, R., & Romeo, D. (1995). Cathelicidins: a novel protein family with a common proregion and a variable C‐terminal antimicrobial domain. FEBS Letters, 374(1), 1-5. DOI:10.1016/0014-5793(95)01050-o

Zhao, C., Wang, I., & Lehrer, R. I. (1996). Widespread expression of beta‐defensin hBD‐1 in human secretory glands and epithelial cells. FEBS Letters, 396(2-3), 319-322. DOI:10.1016/0014-5793(96)01123-4