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Samsum ant venom protects against carbon tetrachloride–induced acute spleen toxicity in vivo

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Abstract

Many active molecules used in the development of new drugs are produced by ants. Present study assessed antioxidant and anti-inflammatory properties of Samsum ant venom (SAV) extract in carbon tetrachloride (CCL4)–induced spleen toxicity. Toxicity and oxidative stress were measured in four experimental groups: a negative control group without any treatment, a positive control group (CCl4-treated rats; a single dose of 1 ml/kg CCL4), an experimental group of CCl4-treated rats co-treated daily with SAV (100 μl), and a group to determine safe use with rats treated only with SAV (100 μl) daily for 3 weeks. CCl4-treatment led to an elevation in toxicity and oxidative stress. CCl4 significantly elevated malondialdehyde (MDA) levels, as well as expression of inhibitor of κB (IκB) and tumor necrosis factor-α (TNF-α) proteins. On the other hand, a decrease in glutathione (GSH) and catalase (CAT) levels were detected in CCl4-treated rats. Co-treatment with SAV was found to reduce these inflammatory and oxidative parameters. SAV elucidated a significant recovery of MDA concentration as well as a significant restoration in GSH levels compared to CCl4-treated rats; however, SAV increased CAT levels compared to normal rats. Hence, SAV was found to restore splenomegaly induced in CCl4-treated rats. Histopathological analysis also favored the biochemical analysis showing improvement in splenic architecture in CCl4 and SAV co-treated rats. The antioxidant properties of SAV may potentially enhance anti-inflammatory actions and improve spleen structure and function in CCl4-challenged rats.

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Data availability

The data used to support the findings of this study are included in the article. All data used in this article are publicly available and accessible online.

Abbreviations

DPPH:

2,2-diphenyl-1-picrylhydrazyl

GSH:

glutathione

MDA:

malondialdehyde

SAV:

Samsum ant venom

CAT:

catalase

CCL4 :

carbon tetrachloride

IkB:

inhibitor of kB kinase

FAS:

cell surface death receptor

GAPDH:

glyceraldehyde-3-Phosphate Dehydrogenase

TNF-α:

tumor necrosis factor-α

IL4:

interleukin 4

References

  • AlAnazi M, AlAshahrani M, AlSalamah M (2009) Black ant stings caused by Pachycondyla sennaarensis: a significant health hazard. Ann Saudi Med 29:207–211

    Google Scholar 

  • Alhazza IM, Ebaid H, Abdel-Salam B, Al-Tamimi JH, Hassan I, Rady AM, Mashaly AMA (2019) Thymoquinone ameliorates Pachycondyla sennaarensis venom-induced acute toxic shock in male rats. BMC Pharmacol Toxicol 20:84

    CAS  Google Scholar 

  • Al-Khalifa MS, Ahmed AM, Mashaly AMA, Al-Mekhalfi FA, Khalil G, Siddiqui MI, Ali MF (2010) Studies on the distribution of Pachycondyla Senna arensis (Hymenoptera: Formicidae: Ponerinae) in Saudi Arabia. Ar-Riyadh Region. Pak J Zool 42:707–713

    Google Scholar 

  • Al-Khalifa MS, Mashaly AMA, Siddiqui MI, Al-Mekhlafi FA (2015) Samsum ant, Brachyponera sennaarensis (Formicidae: Ponerinae): distribution and abundance in Saudi Arabia. Saudi J Biol Sci 22:575–579

    Google Scholar 

  • Al-Tamimi J, Alhazza IM, Al-Khalifa M, Metwalli A, Rady A, Ebaid H (2016) Potential effects of samsum ant, Brachyponera sennaarensis, venom on TNF-α/NF-κB mediated inflammation in CCL4-toxicity in vivo. Lipids Health Dis 15:1–11

    Google Scholar 

  • Al-Tamimi J, Semlali A, Hassan I, Ebaid H, Alhazza IM, Mehdi SH, Al-Khalifa M, Alanazi MS (2018) Samsum ant venom exerts anticancer activity through immunomodulation in vitro and in vivo. Cancer Biother Radiopharm 33:65–73

    CAS  Google Scholar 

  • Andriţoiu CV, Andriţoiu V, Cuciureanu M, Nica-Badea D, Bibire N, Popa M (2014) Effect of apitherapy products against carbon tetrachloride-induced toxicity in Wistar rats. Romanian J Morphol Embryol 55:835–847

    Google Scholar 

  • Awaad A (2015) Histopathological and immunological changes induced by magnetite nanoparticles in the spleen, liver and genital tract of mice following intravaginal instillation. J Basic Appl Zool 71:32–47

    CAS  Google Scholar 

  • Bancroft JD, Layton C (2012) The hematoxylin and eosin. Bancroft’s theory and practice of histological techniques, expert consult: online and print. 7th edn. Amsterdam, Netherlands: 173

  • Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181:1199–1200

    CAS  Google Scholar 

  • Chehl N, Chipitsyna G, Gong Q, Yeo CJ, Arafat HA (2009) Anti-inflammatory effects of the Nigella sativa seed extract, thymoquinone, in pancreatic cancer cells. Hpb (Oxford) 11(5):373–381

    Google Scholar 

  • Chen S (1992) Effects of spleen on inducing portal hypertension and liver cirrhosis in rats. Zhonghua Yi Xue Za Zhi 72:338–381

    CAS  Google Scholar 

  • Collingwood CA (1985) Hymenoptera: Fam. Formicidae of Saudi Arabia. Fauna Saudi Arabia 7:230–302

    Google Scholar 

  • Dommels YE, Butts CA, Zhu S, Davy M, Martell S, Hedderley D, Barnett MP, McNabb WC, Roy NC (2007) Characterization of intestinal inflammation and identification of related gene expression changes in mdr1a mice. Genes Nutr 2:209–223

    CAS  Google Scholar 

  • Dong S, Chen QL, Song YN, Sun Y, Wei B, Li XY, Hu YY, Liu P, Su SB (2016) Mechanisms of CCl4-induced liver fibrosis with combined transcriptomic and proteomic analysis. J Toxicol Sci 41:561–572

    CAS  Google Scholar 

  • Ebaid H, Al-Khalifa M, Isa AM, Gadoa S (2012) Bioactivity of Samsum ant (Pachycondyla sennaarensis) venom against lipopolysaccharides through antioxidant and upregulation of Akt1 signalling in rats. Lipids Health Dis 11(1):93

    Google Scholar 

  • Ebaid H, Bashandy S, Alhazza I, Rady A, El-Shehry S (2013) Folic acid and melatonin ameliorate carbon tetrachloride-induced hepatic injury, oxidative stress and inflammation in rats. Nutr Metab 10(1):20

    CAS  Google Scholar 

  • Ebaid H, Al-Tamimi J, Hassan I, Alhazza I, Al-Khalifa M (2014) Antioxidant bioactivity of Samsum ant ( Pachycondyla sennaarensis ) venom protects against CCL4 -induced nephrotoxicity in mice. Oxidative Med Cell Longev:1–8

  • Ebaid H, Abdel-Salam B, Alhazza I, Al-Tamimi J, Hassan I, Rady A, Mashaly A, Mahmoud A, Sammour R (2019) Samsum ant venom modulates the immune response and redox status at the acute toxic dose in vivo. J Venomous Anim Toxins Incl Trop Dis 25:e20190020

    CAS  Google Scholar 

  • Ebaid H, Habila M, Hassan I, Al-Tamimi J, Omar MS, Rady A, Alhazza I (2020) Curcumin-containing silver nanoparticles prevent carbon tetrachlorideinduced hepatotoxicity in mice. Comb Chem High Throughput Screen 23:1–11

    Google Scholar 

  • Fortea JI, Fernandez-Mena C, Puerto M, Ripoll C, Almagro J, Banares J, Bellon JM, Banares R, Vaquero J (2018) Comparison of two protocols of carbon tetrachloride-induced cirrhosis in rats-improving yield and reproducibility. Sci Rep 8:9163

    Google Scholar 

  • Heinen TE, da Veiga ABG (2011) Arthropod venoms and cancer. Toxicon 57:497–511

    CAS  Google Scholar 

  • Jiang L, Huang J, Wang Y, Tang H (2012) Metabonomic analysis reveals the CCl4-induced systems alterations for multiple rat organs. J Proteome Res 11:3848–3859

    CAS  Google Scholar 

  • Jungmin L (2016) Further research on the biological activities and the safety of raspberry ketone is needed. NFS Journal 2:15–18

    Google Scholar 

  • Khalil SR, Abd-Elhakim YM, Selim ME, Al-Ayadhi LY (2015) Apitoxin protects rat pups brain from propionic acid-induced oxidative stress: the expression pattern of Bcl-2 and Caspase-3 apoptotic genes. Neurotoxicology 49:121–131

    CAS  Google Scholar 

  • Khan RA, Khan MR, Sahreen S (2012) CCl4-induced hepatotoxicity: protective effect of rutin on p53, CYP2E1 and the antioxidative status in rat. BMC Complement Altern Med 12:178

    Google Scholar 

  • Kotb M, Calandra T (2003) Cytokines and chemokines in infectious diseases handbook. Humana Press, Totowa

    Google Scholar 

  • Kowalski J, Blada P, Kucia K, Madej A, Herman ZS (2001) Neuroleptics normalize increased release of interleukin- 1beta and tumor necrosis factoralpha from monocytes in schizophrenia. Schizophr Res 50:169–175

    CAS  Google Scholar 

  • Kuriakose GC, Kurup GM (2008) Antioxidant activity of Aulosira fertilisima on CCl 4 induced hepatotoxicity in rats. Indian J Exp Biol 46:52–59

    Google Scholar 

  • Lee SH, Choi SM, Yang EJ (2015) Bee venom acupuncture augments anti-inflammation in the peripheral organs of hSOD1G93A transgenic mice. Toxins 7:2835–2844

    CAS  Google Scholar 

  • Lim Y, Levy M, Bray TM (2004) Dietary zinc alters early inflammatory responses during cutaneous wound healing in weanling CD-1 mice. J Nutr 134:811–816

    CAS  Google Scholar 

  • Lin X, Huang R, Zhang S, Zheng L, Wei L, He M, Zhou Y, Zhuo L, Huang Q (2012) Methyl helicterate protects against CCl4-induced liver injury in rats by inhibiting oxidative stress, NF-κB activation, Fas/FasL pathway and cytochrome P4502E1 level, Fas. Food Chem Toxicol 50:3413–3420

    CAS  Google Scholar 

  • Liu Y, Meyer C, Xu C, Weng H, Hellerbrand C, ten Dijke P, Dooley S (2013) Animal models of chronic liver diseases. Am J Physiol Gastrointest Liver Physiol 304:449–468

    Google Scholar 

  • Manibusan MK, Odin M, Eastmond DA (2007) Postulated carbon tetrachloride mode of action: a review. J Environ Sci Health C 25:185–209

    CAS  Google Scholar 

  • Mashaly AM, Ahmed AM, Al-Abdullah MA, Al-Khalifa MS (2011) The trail pheromone of the venomous samsum ant, Pachycondyla sennaarensis. J Insect Sci 11:31

    Google Scholar 

  • Mebius RE, Kraal G (2005) Structure and function of the spleen. Nat Rev Immunol 5:606–616

    CAS  Google Scholar 

  • Merra E, Calzaretti G, Bobba A, Storelli MM, Casalino E (2014) Antioxidant role of hydroxytyrosol on oxidative stress in cadmium-intoxicated rats: different effect in spleen and testes. Drug Chem Toxicol 37:420–426

    CAS  Google Scholar 

  • Metsamuuronen S, Siren H (2019) Bioactive phenolic compounds, metabolism and properties: a review on valuable chemical compounds in Scots pine and Norway spruce. Phytochem Rev 18:623–664

    CAS  Google Scholar 

  • Morgan ED (2008) Chemical sorcery for sociality: exocrine secretions of ants (Hymenoptera: Formicidae). Myrmecol News 11:79–90

    Google Scholar 

  • Nagata S (1997) Apoptosis by death factor. Cell 88:355–365

    CAS  Google Scholar 

  • Nikbakhtzadeh MR, Akbarzadeh K, Tirgari S (2009) Bioecology and chemical diversity of abdominal glands in the Iranian samsum ant Pachycondyla sennaarensis (Formicidae: Ponerinae). J Venom Anim Toxins incl Trop Dis 15:509–526

    CAS  Google Scholar 

  • Noel G, Guo X, Wang Q, Schwemberger S, Byrum D, Ogle C (2007) Postburn monocytes are the major producers of TNF-α in the heterogeneous splenic macrophage population. Shock 27:312–319

    CAS  Google Scholar 

  • Patella V, Incorvaia C, Minciullo PL, Oricchio C, Saitta S, Florio G, Saija A, Gangemi S (2015) Oxidative stress markers in patients with hymenoptera venom allergy. Allergy Asthma Proc 36:9–13

    Google Scholar 

  • Srivastava A, Shivanandappa T (2010) Hepatoprotective effect of the root extract of Decalepis hamiltonii against carbon tetrachloride-induced oxidative stress in rat. Food Chem 118:411–417

    CAS  Google Scholar 

  • Suh SJ, Kim KS, Kim MJ, Chang YC, Lee SD, Kim MS, Kwon DY, Kim CH (2006) Effects of bee venom on protease activities and free radical damages in synovial fluid from type II collagen-induced rheumatoid arthritis rats. Toxicol in Vitro 20:1465–1471

    CAS  Google Scholar 

  • Wu X, Cao W, Jia G, Zhao H, Chen X, Wu C, Tang J, Wang J, Liu G (2017) New insights into the role of spermine in enhancing the antioxidant capacity of rat spleen and liver under oxidative stress. Anim Nutr 3:85–90

    Google Scholar 

  • Zhang M, Luo J, Zhang C, Cao H, Xia B, Hu G (2017) Alterations in antioxidant function and cell apoptosis in duck spleen exposed to molybdenum and/or cadmium. J Vet Sci 18:193–200

    Google Scholar 

  • Zhao Y, Wang X, Kawai M, Liu J, Liu M, Mori A (1995) Antioxidant activity of Chinese ant extract preparations. Acta Med Okayama 49:275–279

    CAS  Google Scholar 

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Acknowledgements

The authors also acknowledge the Deanship of Scientific Research at King Saud University.

Funding

This study is supported by the Deanship of Scientific Research at King Saud University through the Research group Project No. RG-1436-004.

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Authors and Affiliations

  1. Department of Zoology, College of Science, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    Jameel Al-Tamimi, Hossam Ebaid, Iftekhar Hassan, Ibrahim M. Alhazza, Waleed Hailan & Mohammed Al-Khalifa

Authors
  1. Jameel Al-Tamimi
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  2. Hossam Ebaid
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  3. Iftekhar Hassan
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  4. Ibrahim M. Alhazza
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  5. Waleed Hailan
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  6. Mohammed Al-Khalifa
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Contributions

Jameel Al-Tamimi and Hossam Ebaid conceived the research idea and write introduction and Discussion. Jameel Al-Tamimi had extracted the ant venom and treated the rats. All the biochemical and immunological experiments were conducted by Jameel Al-Tamimi and Iftekhar Hassan. All the results, figures and gene expression data were prepared by Iftekhar Hassan and Waleed Hailan. Hossam Ebaid analyzed the whole histological study. Jameel Al-Tamimi drafted the manuscript while results were analyzed by Hossam Ebaid, Iftekhar Hassan, Ibrahim M Alhazza, Waleed Hailan and Mohammed Al-Khalifa. All the authors have approved the manuscript.

Corresponding author

Correspondence to Ibrahim M. Alhazza.

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The authors declare that they have no competing interests.

Ethical approval and consent to participate

All procedures were conducted in accordance with guidelines for the care and use of experimental animals by the Committee for the Purpose of Control and Supervision of Experiments on Animals and the National Institutes of Health.

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The authors generated all of all the data from our own experiments conducted in the laboratory. We have all consented to the publication of the data presented in this manuscript.

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Responsible Editor: Mohamed M. Abdel-Daim

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Al-Tamimi, J., Ebaid, H., Hassan, I. et al. Samsum ant venom protects against carbon tetrachloride–induced acute spleen toxicity in vivo. Environ Sci Pollut Res 28, 31138–31150 (2021). https://doi.org/10.1007/s11356-020-12252-3

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