Anti-inflammatory activity and structure-activity relationships of brominated indoles from a marine mollusc

Article

Ahmad, Tarek B., Rudd, David, Smith, Joshua, Kotiw, Michael, Mouatt, Peter, Seymour, Lisa M., Liu, Lei and Benkendorff, Kirsten. 2017. "Anti-inflammatory activity and structure-activity relationships of brominated indoles from a marine mollusc." Marine Drugs. 15 (5), pp. 1-19. https://doi.org/10.3390/md15050133
Article Title

Anti-inflammatory activity and structure-activity relationships of brominated indoles from a marine mollusc

ERA Journal ID14994
Article CategoryArticle
AuthorsAhmad, Tarek B. (Author), Rudd, David (Author), Smith, Joshua (Author), Kotiw, Michael (Author), Mouatt, Peter (Author), Seymour, Lisa M. (Author), Liu, Lei (Author) and Benkendorff, Kirsten (Author)
Journal TitleMarine Drugs
Journal Citation15 (5), pp. 1-19
Article Number133
Number of Pages19
Year2017
Place of PublicationBasel, Switzerland
ISSN1660-3397
Digital Object Identifier (DOI)https://doi.org/10.3390/md15050133
Web Address (URL)http://www.mdpi.com/1660-3397/15/5/133
Abstract

Marine molluscs are rich in biologically active natural products that provide new potential sources of anti-inflammatory agents. Here we used bioassay guided fractionation of extracts from the muricid Dicathais orbita to identify brominated indoles with anti-inflammatory activity, based on the inhibition of nitric oxide (NO) and tumour necrosis factor (TNF) in lipopolysaccharide (LPS)
stimulated RAW264.7 macrophages and prostaglandin E2 (PGE2) in calcium ionophore-stimulated 3T3 ccl-92 fibroblasts. Muricid brominated indoles were then compared to a range of synthetic indoles to determine structure-activity relationships. Both hypobranchial gland and egg extracts inhibited the production of NO significantly with IC50 of 30.8 and 40 ug/mL, respectively. The hypobranchial gland extract also inhibited the production of TNFa and PGE2 with IC50 of 43.03 ug/mL and 34.24 ug/mL, respectively. The purified mono-brominated indole and isatin compounds showed
significant inhibitory activity against NO, TNFa, and PGE2, and were more active than dimer indoles and non-brominated isatin. The position of the bromine atom on the isatin benzene ring significantly affected the activity, with 5Br > 6Br > 7Br. The mode of action for the active hypobranchial gland extract, 6-bromoindole, and 6-bromoisatin was further tested by the assessment of the translocation of nuclear factor kappa B (NFkB) in LPS-stimulated RAW264.7 mouse macrophage. The extract
(40 ug/mL) significantly inhibited the translocation of NFkB in the LPS-stimulated RAW264.7 macrophages by 48.2%, whereas 40 ug/mL of 6-bromoindole and 6-bromoistain caused a 60.7% and 63.7% reduction in NFkB, respectively. These results identify simple brominated indoles as useful
anti-inflammatory drug leads and support the development of extracts from the Australian muricid D. orbita, as a new potential natural remedy for the treatment of inflammation.

Keywordsmarine natural products; inflammation; NO inhibition; Muricidae; isatin; Tyrian purple
ANZSRC Field of Research 2020420899. Traditional, complementary and integrative medicine not elsewhere classified
Byline AffiliationsSouthern Cross University
Centre for Health Sciences Research
Institution of OriginUniversity of Southern Queensland
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Seymour, Lisa M., Falconer, Linda, Deutscher, Ania T., Minion, F. Chris, Padula, Matthew P., Dixon, Nicholas E., Djordjevic, Steven P. and Walker, Mark J.. 2011. "Mhp107 is a member of the multifunctional adhesin family of Mycoplasma hyopneumoniae." Journal of Biological Chemistry. 286 (12), pp. 10097-10104. https://doi.org/10.1074/jbc.M110.208140
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Seymour, Lisa M., Jenkins, Cheryl, Deutscher, Ania T., Raymond, Benjamin B. A., Padula, Matthew P., Tacchi, Jessica L., Bogema, Daniel R., Eamens, Graeme J., Woolley, Lauren K., Dixon, Nicholas E., Walker, Mark J. and Djordjevic, Steven P.. 2012. "Mhp182 (P102) binds fibronectin and contributes to the recruitment of plasmin(ogen) to the Mycoplasma hyopneumoniae cell surface." Cellular Microbiology. 14 (1), pp. 81-94. https://doi.org/10.1111/j.1462-5822.2011.01702.x
Characterization of cleavage events in the multifunctional cilium adhesin Mhp684 (P146) reveals a mechanism by which mycoplasma hyopneumoniae regulates surface topography
Bogema, Daniel R., Deutscher, Ania T., Woolley, Lauren K., Seymour, Lisa M., Raymond, Benjamin B. A., Tacchi, Jessica L., Padula, Matthew P., Dixon, Nicholas E., Minion, F. Chris, Jenkins, Cheryl, Walker, Mark J. and Djordjevic, Steven P.. 2012. "Characterization of cleavage events in the multifunctional cilium adhesin Mhp684 (P146) reveals a mechanism by which mycoplasma hyopneumoniae regulates surface topography." mBio. 3 (2), pp. 1-12. https://doi.org/10.1128/mBio.00282-11
Repeat regions R1 and R2 in the P97 paralogue Mhp271 of Mycoplasma hyopneumoniae bind heparin, fibronectin and porcine cilia
Deutscher, Ania T., Jenkins, Cheryl, Minion, F. Chris, Seymour, Lisa M., Padula, Matthew P., Dixon, Nicholas E., Walker, Mark J. and Djordjevic, Steven P.. 2010. "Repeat regions R1 and R2 in the P97 paralogue Mhp271 of Mycoplasma hyopneumoniae bind heparin, fibronectin and porcine cilia." Molecular Microbiology. 78 (2), pp. 444-458. https://doi.org/10.1111/j.1365-2958.2010.07345.x
A processed multidomain hyopneumoniae adhesin binds fibronectin, plasminogen and swine respiratory cilia
Seymour, Lisa M., Deutscher, Ania T., Jenkins, Cheryl, Kuit, Tracey A., Falconer, Linda, Minion, F. Chris, Crossett, Ben, Padula, Matthew, Dixon, Nicholas E., Djordjevic, Steven P. and Walker, Mark J.. 2010. "A processed multidomain hyopneumoniae adhesin binds fibronectin, plasminogen and swine respiratory cilia." Journal of Biological Chemistry. 285 (44), pp. 33971-33978. https://doi.org/10.1074/jbc.M110.104463
The globally disseminated M1T1 clone of Group A streptococcus evades autophagy for intracellular replication
Barnett, Timothy C., Liebl, David, Seymour, Lisa M., Gillen, Christine M., Yan Lim, Jin, LaRock, Christopher N., Davies, Mark R., Schulz, Benjamin L., Nizet, Victor, Teasdale, Rohan D. and Walker, Mark J.. 2013. "The globally disseminated M1T1 clone of Group A streptococcus evades autophagy for intracellular replication." Cell Host and Microbe. 14 (6), pp. 675-682. https://doi.org/10.1016/j.chom.2013.11.003
The diversity and antimicrobial activity of Preussia sp. Endophytes isolated from Australian dry rainforests
Mapperson, Rachel R., Kotiw, Michael, Davis, Rohan A. and Dearnaley, John D. W.. 2014. "The diversity and antimicrobial activity of Preussia sp. Endophytes isolated from Australian dry rainforests." Current Microbiology: an international journal. 68 (1), pp. 30-37. https://doi.org/10.1007/s00284-013-0415-5
Immunological response to parenteral vaccination with recombinant hepatitis B virus surface antigen virus-like particles expressing Helicobacter pylori KatA epitopes in a murine H. pylori challenge model
Kotiw, Michael, Johnson, Megan, Pandey, Manisha, Fry, Scott, Hazell, Stuart L., Netter, Hans J., Good, Michael F. and Olive, Colleen. 2012. "Immunological response to parenteral vaccination with recombinant hepatitis B virus surface antigen virus-like particles expressing Helicobacter pylori KatA epitopes in a murine H. pylori challenge model ." Clinical and Vaccine Immunology. 19 (2), pp. 268-276. https://doi.org/10.1128/CVI.05295-11
Ravenic acid, a new tetramic acid isolated from a cultured microfungus, penicillium sp.
Michael, Adam P., Grace, Emily J., Kotiw, Mike and Barrow, Russell A.. 2002. "Ravenic acid, a new tetramic acid isolated from a cultured microfungus, penicillium sp." Journal of Natural Products. 65 (9), pp. 1360-1362. https://doi.org/10.1021/np0200358
Xanthones from a microfungus of the genus Xylaria
Healy, Peter C., Hocking, Ailsa, Tran-Dinh, Nai, Pitt, John I., Shivas, Roger G., Mitchell, Jennifer K., Kotiw, Mike and Davis, Rohan A.. 2004. "Xanthones from a microfungus of the genus Xylaria." Phytochemistry: the international journal of plant chemistry, plant biochemistry and molecular biology. 65 (16), pp. 2373-2378. https://doi.org/10.1016/j.phytochem.2004.07.019
Phomoxins B and C: polyketides from an endophytic fungus of the genus eupenicillium
Davis, Rohan A., Andjic, Vesna, Kotiw, Michael and Shivas, Roger G.. 2005. "Phomoxins B and C: polyketides from an endophytic fungus of the genus eupenicillium." Phytochemistry: the international journal of plant chemistry, plant biochemistry and molecular biology. 66 (23), pp. 2771-2775. https://doi.org/10.1016/j.phytochem.2005.09.004
A RAPD-PCR genotyping assay which correlates with serotypes of group B streptococci
Zhang, G. W., Kotiw, M. and Daggard, G.. 2002. "A RAPD-PCR genotyping assay which correlates with serotypes of group B streptococci." Letters in Applied Microbiology. 35 (3), pp. 247-250. https://doi.org/10.1046/j.1472-765X.2002.01177.x
Late-onset and recurrent neonatal group B streptococcal disease associated with breast milk transmission
Kotiw, Michael, Zhang, Gwang W., Daggard, Grant, Reiss-Levy, Elizabeth, Tapsall, John W. and Numa, Andrew. 2003. "Late-onset and recurrent neonatal group B streptococcal disease associated with breast milk transmission." Pediatric and Developmental Pathology. 6 (3), pp. 251-256. https://doi.org/10.1007/s10024-001-0276-y
Synthesis of the fungal natural product (-)-xylariamide A
Kotiw, Michael and Davis, Rohan A.. 2005. "Synthesis of the fungal natural product (-)-xylariamide A." Tetrahedron Letters: the international journal for the rapid publication of all preliminary communications in organic chemistry. 46 (31), pp. 5199-5201. https://doi.org/10.1016/j.tetlet.2005.05.114
Caelestines A-D, Brominated Quinolinecarboxylic Acids from the Australian Ascidian Aplidium caelestis
Yin, Sheng, Boyle, Glen M., Carroll, Anthony R., Kotiw, Michael, Dearnaley, John, Quinn, Ronald J. and Davis, Rohan A.. 2010. "Caelestines A-D, Brominated Quinolinecarboxylic Acids from the Australian Ascidian Aplidium caelestis." Journal of Natural Products. 73 (9), pp. 1586-1589. https://doi.org/10.1021/np100329w
Detection of anti-TNFα activity in canine hyperimmune serum using a TNFα inhibition assay
Kotiw, Michael, Morgan, Michael, Taylor, Stephen M. and Shiels, Ian A.. 2010. "Detection of anti-TNFα activity in canine hyperimmune serum using a TNFα inhibition assay ." Veterinary Clinical Pathology. 39 (1), pp. 46-52. https://doi.org/10.1111/j.1939-165X.2009.00166.x
Anti-inflammatory activity of hyperimmune plasma in a lipopolysaccharide-mediated rat air pouch model of inflammation
Essien, Bryan E. and Kotiw, Michael. 2012. "Anti-inflammatory activity of hyperimmune plasma in a lipopolysaccharide-mediated rat air pouch model of inflammation." Inflammation. 35 (1), pp. 58-64. https://doi.org/10.1007/s10753-010-9289-x
Effect of canine hyperimmune plasma on TNFa and inflammatory cell levels in a lipopolysaccharide-mediated rat air pouch model of inflammation
Strunin, Dmitry, Essien, Bryan, Kotiw, Michael and Butler, Harry. 2009. "Effect of canine hyperimmune plasma on TNFa and inflammatory cell levels in a lipopolysaccharide-mediated rat air pouch model of inflammation." Reinhart, Konrad (ed.) Sepsis 2009: Critical Care Conference. Amsterdam, Netherlands 11 - 14 Nov 2009 https://doi.org/10.1186/cc8064
A mathematical model to account for quantitative iterative effect of TNF-α positive feedback mechanism on inflammatory cascade in TLR-4 mediated TNF-α signaling pathway
Roberts, Tony, Essien, Bryan, Kotiw, Michael, Butler, Harry and Strunin, Dmitry. 2008. "A mathematical model to account for quantitative iterative effect of TNF-α positive feedback mechanism on inflammatory cascade in TLR-4 mediated TNF-α signaling pathway." Ragan, Mark (ed.) 19th International Conference on Genome Informatics (GIW 2008). Gold Coast, Australia 01 - 03 Dec 2008 London, United Kingdom.
In vitro effect of canine hyperimmune sera on TNFa activity
Kotiw, Michael, Shiels, I. A., Wilson, R. P. and Reeve-Johnson, Lloyd. 2006. "In vitro effect of canine hyperimmune sera on TNFa activity." Journal of Veterinary Pharmacology and Therapeutics. 29 (Supplement 1), pp. 100-101. https://doi.org/10.1111/j.1365-2885.2006.00761.x
The effect of equine hyperimmune sera on TNF alpha activity in a L929 cell bioassay
Kotiw, M., Raghaven, C., Johnson, M., Shiels, I. A. and Wilson, R. P.. 2006. "The effect of equine hyperimmune sera on TNF alpha activity in a L929 cell bioassay." Bryden, W. L. (ed.) AESS 2006: Australian Equine Science Symposium: Research for the 21st Century Horse Industry: From Genomics to the Winning Post. Gold Coast, Australia 13 - 14 Jun 2006 Gold Coast, Australia.
Biological methods: a novel course in undergraduate biology
Kotiw, Michael, Learmonth, Robert P. and Sutherland, Mark W.. 1999. "Biological methods: a novel course in undergraduate biology." Biochemical Education. 27 (3), pp. 131-134. https://doi.org/10.1016/S0307-4412(99)00002-3
The relevance of human rights to health status in Australian Aboriginal and Torres Strait Islander communities
Smallwood, Gracelyn, White, Colin and Kotiw, Michael. 1997. "The relevance of human rights to health status in Australian Aboriginal and Torres Strait Islander communities." Health and Human Rights: an international journal. 2 (2), pp. 127-136.
In vitro and in vivo determination of ant-TNFa activity in canine plasma from donors subject to pre conditioning with endotoxin
Kotiw, Michael, Morgan, Michael, Lopez, Jesus, Taylor, Steven and Shiels, Ian. 2007. "In vitro and in vivo determination of ant-TNFa activity in canine plasma from donors subject to pre conditioning with endotoxin." Marshall, John (ed.) SEPSIS 2007: International Sepsis Forum ISF . Paris, France 26 - 29 Sep 2007 London, United Kingdom. https://doi.org/10.1186/cc6002
In the footsteps of Florey: utilising cultured microfungi in the search for new antibiotics
Parker, C., Barrow, Russell, Bloor, S. J., Grace, Emily J., Michael, Adam P., Thompson, Christopher and Kotiw, Michael. 2001. "In the footsteps of Florey: utilising cultured microfungi in the search for new antibiotics." Bernhardt, Debra (ed.) FACS 2001: 9th Asian Chemical Congress . Brisbane, Australia 02 - 04 Jul 2001 Brisbane, Australia.
Exploring the potential for dual vaccination against Hepatitis B virus and Helicobacter pylori using a recombinant virus like particle
Kotiw, Michael, Olive, C., Johnson, Megan, Pandy, M., Fry, Scott Robert, Hazell, Stuart L., Netter, H. and Good, M.. 2006. "Exploring the potential for dual vaccination against Hepatitis B virus and Helicobacter pylori using a recombinant virus like particle." Sirtori, Patrizia (ed.) 6th National Congress of the Italian Society of Virology - a joint meeting with the Virus Group of the Society for General Microbiology (UK). Orvieto, Italy 18 - 20 Sep 2006 Italy.
Isochromophilone IX, a novel GABA-containing metabolite isolated from a cultured fungus, Penicillium sp.
Michael, Adam P., Grace, Emily J., Kotiw, Michael and Barrow, Russell A.. 2003. "Isochromophilone IX, a novel GABA-containing metabolite isolated from a cultured fungus, Penicillium sp." Australian Journal of Chemistry: an international journal for chemical science. 56 (1), pp. 13-15. https://doi.org/10.1071/CH02021