Skip to main content
SpringerLink
Log in

Anticolitic activity of prodigiosin loaded with selenium nanoparticles on acetic acid–induced colitis in rats

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Ulcerative colitis (UC) is a chronic autoimmune inflammatory disease associated with extensive mucosal damage. Prodigiosins (PGs) are natural bacterial pigments with well-known antioxidant and immunosuppressive properties. In the current study, we examined the possible protective effect of PGs loaded with selenium nanoparticles (PGs-SeNPs) against acetic acid (AcOH)-induced UC in rats. Thirty-five rats were separated into five equal groups with seven animals/group: control, UC, PGs (300 mg/kg), sodium selenite (Na2SeO3, 2 mg/kg), PGs-SeNPs (0.5 mg/kg), and 5-aminosalicylates (5-ASA, 200 mg/kg). Interestingly, PGs-SeNPs administration lessened colon inflammation and mucosal damage as indicated by inhibiting inflammatory markers upon AcOH injection. Furthermore, PGs-SeNPs improved the colonic antioxidant capacity and prevented oxidative insults as evidenced by the upregulation of Nrf2- and its downstream antioxidants along with the decreased pro-oxidants [reactive oxygen species (ROS), carbonyl protein, malondialdehyde (MDA), inducible nitric oxide synthase (iNOS), and nitric oxide (NO] in the colon tissue. Furthermore, PGs-SeNPs protected intestinal cell loss through blockade apoptotic cascade by decreasing pro-apoptotic proteins [Bcl-2-associated X protein (Bax) and caspase-3] and increasing anti-apoptotic protein, B cell lymphoma 2 (Bcl2). Collectively, PGs-SeNPs could be used as an alternative anti-colitic option due to their strong anti-inflammatory, antioxidant, and anti-apoptotic activities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

All relevant data are within the paper.

References

  • Abdel-Daim MM, Eissa IA, Abdeen A, Abdel-Latif HM, Ismail M, Dawood MA, Hassan AM (2019) Lycopene and resveratrol ameliorate zinc oxide nanoparticles-induced oxidative stress in Nile tilapia, Oreochromis niloticus. Environ Toxicol Pharmacol 69:44–50

    Article  CAS  Google Scholar 

  • Abdel Moneim AE (2016) Indigofera oblongifolia prevents lead acetate-induced hepatotoxicity, oxidative stress, fibrosis and apoptosis in rats. PLoS ONE 11:e0158965

    Article  CAS  Google Scholar 

  • Abdelfattah MS, Elmallah MI, Ebrahim HY, Almeer RS, Eltanany RM, Abdel Moneim AE (2019) Prodigiosins from a marine sponge-associated actinomycete attenuate HCl/ethanol-induced gastric lesion via antioxidant and anti-inflammatory mechanisms. PLoS ONE 14:e0216737

    Article  CAS  Google Scholar 

  • Abraham C (2009): ChoJH. Inflammatory bowel disease 361, 2066-2078

  • Adedara IA, Fabunmi AT, Ayenitaju FC, Atanda OE, Adebowale AA, Ajayi BO, Owoeye O, Rocha JB, Farombi EO (2020) Neuroprotective mechanisms of selenium against arsenic-induced behavioral impairments in rats. Neurotoxicology 76:99–110

    Article  CAS  Google Scholar 

  • Al-Brakati A, Alsharif KF, Alzahrani KJ, Kabrah S, Al-Amer O, Oyouni AA, Habotta OA, Lokman MS, Bauomy AA, Kassab RB (2021) Using green biosynthesized lycopene-coated selenium nanoparticles to rescue renal damage in glycerol-induced acute kidney injury in rats. Int J Nanomed 16:4335

    Article  Google Scholar 

  • Alajmi RA, Al-Megrin WA, Metwally D, Al-Subaie H, Altamrah N, Barakat AM, Abdel Moneim AE, Al-Otaibi TT, El-Khadragy M (2019): Anti-toxoplasma activity of silver nanoparticles green synthesized with Phoenix dactylifera and Ziziphus spina-christi extracts which inhibits inflammation through liver regulation of cytokines in Balb/c mice. Biosci Rep 39

  • AlBasher G, Alfarraj S, Alarifi S, Alkhtani S, Almeer R, Alsultan N, Alharthi M, Alotibi N, Al-Dbass A, Moneim AEA (2020) Nephroprotective role of selenium nanoparticles against glycerol-induced acute kidney injury in rats. Biol Trace Elem Res 194:444–454

    Article  CAS  Google Scholar 

  • Albrakati A, Alsharif KF, Al Omairi NE, Alsanie WF, Almalki ASA, Abd Elmageed ZY, Elshopakey GE, Lokman MS, Bauomy AA, Abdel Moneim AE, Kassab RB (2021) Neuroprotective efficiency of prodigiosins conjugated with selenium nanoparticles in rats exposed to chronic unpredictable mild stress is mediated through antioxidative, anti-inflammatory, anti-apoptotic, and neuromodulatory activities. Int J Nanomed 16:8447

    Article  CAS  Google Scholar 

  • Alkhudhayri A, Al-Shaebi EM, Qasem MA, Murshed M, Mares MM, Al-Quraishy S, Dkhil MA (2020): Antioxidant and anti-apoptotic effects of selenium nanoparticles against murine eimeriosis. Anais da Academia Brasileira de Ciências 92

  • Almeer RS, Mahmoud SM, Amin HK, Moneim AEA (2018) Ziziphus spina-christi fruit extract suppresses oxidative stress and p38 MAPK expression in ulcerative colitis in rats via induction of Nrf2 and HO-1 expression. Food Chem Toxicol 115:49–62

    Article  CAS  Google Scholar 

  • Anissian D, Ghasemi-Kasman M, Khalili-Fomeshi M, Akbari A, Hashemian M, Kazemi S, Moghadamnia AA (2018) Piperine-loaded chitosan-STPP nanoparticles reduce neuronal loss and astrocytes activation in chemical kindling model of epilepsy. Int J Biol Macromol 107:973–983

    Article  CAS  Google Scholar 

  • Araki Y, Mukaisyo K-I, Sugihara H, Fujiyama Y, Hattori T (2010) Increased apoptosis and decreased proliferation of colonic epithelium in dextran sulfate sodium-induced colitis in mice. Oncol Rep 24:869–874

    Article  CAS  Google Scholar 

  • Bedard K, Krause K-H (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245–313

    Article  CAS  Google Scholar 

  • Bradley PP, Priebat DA, Christensen RD, Rothstein G (1982) Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 78:206–209

    Article  CAS  Google Scholar 

  • Che L, Li Y, Song R, Qin C, Hao W, Wang B, Yang L, Peng P, Xu F (2019) Anti-inflammatory and anti-apoptosis activity of taraxasterol in ulcerative colitis in vitro and in vivo. Exp Ther Med 18:1745–1751

    CAS  Google Scholar 

  • Chen J, Li Y, Liu F, Hou D-X, Xu J, Zhao X, Yang F, Feng X (2019) Prodigiosin promotes Nrf2 activation to inhibit oxidative stress induced by microcystin-LR in HepG2 cells. Toxins 11:403

    Article  CAS  Google Scholar 

  • Curkovic I, Egbring M, Kullak-Ublick GA (2013) Risks of inflammatory bowel disease treatment with glucocorticosteroids and aminosalicylates. Dig Dis 31:368–373

    Article  Google Scholar 

  • Dawood MA, Koshio S, Zaineldin AI, Van Doan H, Moustafa EM, Abdel-Daim MM, Angeles Esteban M, Hassaan MS (2019) Dietary supplementation of selenium nanoparticles modulated systemic and mucosal immune status and stress resistance of red sea bream (Pagrus major). Fish Physiol Biochem 45:219–230

    Article  CAS  Google Scholar 

  • de Kinderen RJ, Evers SM, Rinkens R, Postulart D, Vader CI, Majoie MH, Aldenkamp AP (2014) Side-effects of antiepileptic drugs: the economic burden. Seizure 23:184–190

    Article  Google Scholar 

  • Dubinsky MC (2017) Reviewing treatments and outcomes in the evolving landscape of ulcerative colitis. Postgrad Med 129:538–553

    Article  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  Google Scholar 

  • Elmallah MI, Cogo S, Constantinescu AA, Elifio-Esposito S, Abdelfattah MS, Micheau O (2020) Marine actinomycetes-derived secondary metabolites overcome trail-resistance via the intrinsic pathway through downregulation of survivin and XIAP. Cells 9:1760

    Article  CAS  Google Scholar 

  • Factor VM, Kiss A, Woitach JT, Wirth PJ, Thorgeirsson SS (1998) Disruption of redox homeostasis in the transforming growth factor-alpha/c-myc transgenic mouse model of accelerated hepatocarcinogenesis. J Biol Chem 273:15846–15853

    Article  CAS  Google Scholar 

  • Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 126:131–138

    Article  CAS  Google Scholar 

  • Gupta J, Fatima MT, Islam Z, Khan RH, Uversky VN, Salahuddin P (2019) Nanoparticle formulations in the diagnosis and therapy of Alzheimer’s disease. Int J Biol Macromol 130:515–526

    Article  CAS  Google Scholar 

  • Hachiya K, Masuya M, Kuroda N, Yoneda M, Tsuboi J, Nagaharu K, Nishimura K, Shiotani T, Ohishi K, Tawara I (2021) Irbesartan, an angiotensin II type 1 receptor blocker, inhibits colitis-associated tumourigenesis by blocking the MCP-1/CCR2 pathway. Sci Rep 11:1–12

    Article  CAS  Google Scholar 

  • Huh J-E, Yim J-H, Lee H-K, Moon E-Y, Rhee D-K, Pyo S (2007) Prodigiosin isolated from Hahella chejuensis suppresses lipopolysaccharide-induced NO production by inhibiting p38 MAPK, JNK and NF-κB activation in murine peritoneal macrophages. Int Immunopharmacol 7:1825–1833

    Article  CAS  Google Scholar 

  • Jang SE, Hyam S, Han M, Kim SY, Lee BG, Kim DH (2013) Lactobacillus brevis G-101 ameliorates colitis in mice by inhibiting NF-κB, MAPK and AKT pathways and by polarizing M1 macrophages to M2-like macrophages. J Appl Microbiol 115:888–896

    Article  CAS  Google Scholar 

  • Jia L, Xue K, Liu J, Habotta OA, Hu L, Abdel Moneim AE (2020): Anticolitic effect of berberine in rat experimental model: impact of PGE2/p38 MAPK pathways. Mediators Inflamm 2020

  • Jung ES, Jang HJ, Hong EM, Lim HL, Lee SP, Kae SH, Lee J (2020) The protective effect of 5-aminosalicylic acid against non-steroidal anti-inflammatory drug-induced injury through free radical scavenging in small intestinal epithelial cells. Medicina 56:515

    Article  Google Scholar 

  • Kassab RB, Lokman MS, Daabo HM, Gaber DA, Habotta OA, Hafez MM, Zhery AS, Moneim AEA, Fouda MS (2020) Ferulic acid influences Nrf2 activation to restore testicular tissue from cadmium-induced oxidative challenge, inflammation, and apoptosis in rats. J Food Biochem 44:e13505

    Article  CAS  Google Scholar 

  • Kayal M, Shah S (2020) Ulcerative colitis: current and emerging treatment strategies. J Clin Med 9:94

    Article  CAS  Google Scholar 

  • Kędzierska E, Dąbkowska L, Obierzyński P, Polakowska M, Poleszak E, Wlaź P, Szewczyk K, Kotlińska J (2018) Synergistic action of sodium selenite with some antidepressants and diazepam in mice. Pharmaceutics 10:270

    Article  CAS  Google Scholar 

  • Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478

    Article  CAS  Google Scholar 

  • Li Y-h, Zhang M, Xiao H-t, Fu H-b, Ho A, Lin C-y, Huang Y, Lin G, Bian Z-x (2015) Addition of berberine to 5-aminosalicylic acid for treatment of dextran sulfate sodium-induced chronic colitis in C57BL/6 mice. PLoS ONE 10:e0144101

    Article  CAS  Google Scholar 

  • Loeschner K, Hadrup N, Hansen M, Pereira SA, Gammelgaard B, Møller LH, Mortensen A, Lam HR, Larsen EH (2014) Absorption, distribution, metabolism and excretion of selenium following oral administration of elemental selenium nanoparticles or selenite in rats. Metallomics 6:330–337

    Article  CAS  Google Scholar 

  • Lu P-D, Zhao Y-H (2020) Targeting NF-κB pathway for treating ulcerative colitis: comprehensive regulatory characteristics of Chinese medicines. Chin Med 15:15

    Article  CAS  Google Scholar 

  • Luck H (1965) Catalase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 855–888

    Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  Google Scholar 

  • Olén O, Erichsen R, Sachs MC, Pedersen L, Halfvarson J, Askling J, Ekbom A, Sørensen HT, Ludvigsson JF (2020) Colorectal cancer in ulcerative colitis: a Scandinavian population-based cohort study. The Lancet 395:123–131

    Article  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    CAS  Google Scholar 

  • Pedersen J, LaCasse EC, Seidelin JB, Coskun M, Nielsen OH (2014) Inhibitors of apoptosis (IAPs) regulate intestinal immunity and inflammatory bowel disease (IBD) inflammation. Trends Mol Med 20:652–665

    Article  CAS  Google Scholar 

  • Polanczyk-Piechota A, Fichna J (2014): Review article: the role of oxidative stress in pathogenesis and treatment of inflammatory bowel diseases. Naunyn Schmiedeberg's Arch Pharmacol

  • Rawat M, Yadukrishnan P, Kumar N (2018): Mechanisms of action of nanoparticles in living systems, microbial biotechnology in environmental monitoring and cleanup. IGI Global, pp. 220–236

  • Rezayat SM, Dehpour A-R, Motamed SM, Yazdanparast M, Chamanara M, Sahebgharani M, Rashidian A (2018) Foeniculum vulgare essential oil ameliorates acetic acid-induced colitis in rats through the inhibition of NF-kB pathway. Inflammopharmacology 26:851–859

    Article  CAS  Google Scholar 

  • Saxena A, Fayad R, Kaur K, Truman S, Greer J, Carson JA, Chanda A (2017) Dietary selenium protects adiponectin knockout mice against chronic inflammation induced colon cancer. Cancer Biol Ther 18:257–267

    Article  CAS  Google Scholar 

  • Soliman SM, Wadie W, Shouman SA, Ainshoka AA (2018) Sodium selenite ameliorates both intestinal and extra-intestinal changes in acetic acid-induced colitis in rats. Naunyn Schmiedebergs Arch Pharmacol 391:639–647

    Article  CAS  Google Scholar 

  • Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34:497–500

    Article  CAS  Google Scholar 

  • Tripathi K, Feuerstein JD (2019): New developments in ulcerative colitis: latest evidence on management, treatment, and maintenance. Drugs in context 8

  • Vochyánová Z, Pokorná M, Rotrekl D, Smékal V, Fictum P, Suchý P, Gajdziok J, Šmejkal K, Hošek J (2017) Prenylated flavonoid morusin protects against TNBS-induced colitis in rats. PLoS ONE 12:e0182464

    Article  CAS  Google Scholar 

  • Wadhwani SA, Shedbalkar UU, Singh R, Chopade BA (2016) Biogenic selenium nanoparticles: current status and future prospects. Appl Microbiol Biotechnol 100:2555–2566

    Article  CAS  Google Scholar 

  • Wang J, Zhu H, Liu X, Liu Z (2014) N-acetylcysteine protects against cadmium-induced oxidative stress in rat hepatocytes. J Vet Sci 15:485–493

    Article  Google Scholar 

  • Wang Z, Li S, Cao Y, Tian X, Zeng R, Liao D-F, Cao D (2016): Oxidative stress and carbonyl lesions in ulcerative colitis and associated colorectal cancer. Oxid Med Cell Longev 2016

  • Xu C, Qiao L, Ma L, Guo Y, Dou X, Yan S, Zhang B, Roman A (2019) Biogenic selenium nanoparticles synthesized by Lactobacillus casei ATCC 393 alleviate intestinal epithelial barrier dysfunction caused by oxidative stress via Nrf2 signaling-mediated mitochondrial pathway. Int J Nanomed 14:4491

    Article  CAS  Google Scholar 

  • Ya Sklyarov A, Panasyuk N, Fomenko I (2011) Role of nitric oxide-synthase and cyclooxygenase/lipooxygenase systems in development of experimental ulcerative colitis. J Physiol Pharmacol 62:65

    Google Scholar 

  • Yu L, Yan J, Sun Z (2017) D-limonene exhibits anti-inflammatory and antioxidant properties in an ulcerative colitis rat model via regulation of iNOS, COX-2, PGE2 and ERK signaling pathways. Mol Med Rep 15:2339–2346

    Article  CAS  Google Scholar 

  • Yuan X, Fu Z, Ji P, Guo L, Al-Ghamdy AO, Alkandiri A, Habotta OA, Moneim AEA, Kassab RB (2020) Selenium nanoparticles pre-treatment reverse behavioral, oxidative damage, neuronal loss and neurochemical alterations in pentylenetetrazole-induced epileptic seizures in mice. Int J Nanomed 15:6339

    Article  CAS  Google Scholar 

  • Zhang S, Fu J, Dogan B, Scherl EJ, Simpson KW (2018) 5-Aminosalicylic acid downregulates the growth and virulence of Escherichia coli associated with IBD and colorectal cancer, and upregulates host anti-inflammatory activity. J Antibiot 71:950–961

    Article  CAS  Google Scholar 

  • Zhu C, Zhang S, Song C, Zhang Y, Ling Q, Hoffmann PR, Li J, Chen T, Zheng W, Huang Z (2017) Selenium nanoparticles decorated with Ulva lactuca polysaccharide potentially attenuate colitis by inhibiting NF-κB mediated hyper inflammation. J Nanobiotechnology 15:1–15

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the Taif University Researchers Supporting Program (Project number: TURSP-2020/151), Taif University, Saudi Arabia.

Author information

Authors and Affiliations

  1. Department of Zoology and Entomology, Faculty of Science, Helwan University, Cairo, Egypt

    Rami B. Kassab & Ahmed E. Abdel Moneim

  2. Department of Biology, Faculty of Science and Arts, Al-Baha University, Almakhwah, Al-Baha, Saudi Arabia

    Rami B. Kassab

  3. Pharmacology and Toxicology Department, Faculty of Pharmacy, Helwan University, Cairo, Egypt

    Mohamad Elbaz

  4. Princess Margaret Cancer Centre, University Health Network, Toronto, ON, Canada

    Mohamad Elbaz

  5. Department of Biology, Faculty of Sciences, University of Tabuk, Tabuk, Saudi Arabia

    Atif A. A. Oyouni

  6. Genome and Biotechnology Unit, Faculty of Sciences, University of Tabuk, Tabuk, Saudi Arabia

    Atif A. A. Oyouni

  7. Medical Genetics Department, Faculty of Medicine, Umm Al-Qura University, Mecca, Saudi Arabia

    Ahmad H. Mufti

  8. Department of Laboratory Medicine, Security Forces Hospital, Mecca, Saudi Arabia

    Abdulrahman Theyab

  9. Department of Human Anatomy, College of Medicine, Taif University, Taif, Saudi Arabia

    Ashraf Al-Brakati

  10. Chemistry Department, Faculty of Science, Helwan University, Cairo, Egypt

    Hala A. Mohamed, Ali M. S. Hebishy, Mohammed I. Y. Elmallah & Mohamed S. Abdelfattah

Authors
  1. Rami B. Kassab
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohamad Elbaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Atif A. A. Oyouni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ahmad H. Mufti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abdulrahman Theyab
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ashraf Al-Brakati
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hala A. Mohamed
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ali M. S. Hebishy
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mohammed I. Y. Elmallah
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Mohamed S. Abdelfattah
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ahmed E. Abdel Moneim
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Rami B. Kassab and Ahmed E. Abdel Moneim designed the project. Hala A. Mohamed, Ali M.S. Hebishy, Mohammed I.Y. Elmallah, and Mohamed S. Abdelfattah performed the experiments. Atif A.A. Oyouni, Ahmad H. Mufti, Abdulrahman Theyab, and Ashraf Al-Brakati analyzed and interpreted the data. Mohamad Elbaz drafted the manuscript. Rami B. Kassab edited the manuscript. Atif A.A. Oyouni, Ahmad H. Mufti, and Abdulrahman Theyab supplied the chemicals and reagents. All authors read and approved the final draft.

Corresponding author

Correspondence to Ahmed E. Abdel Moneim.

Ethics declarations

Ethics approval

The experiments were implemented according to the National Institutes of Health (NIH) Guidelines for the Care and Use of Laboratory Animals, 8th edition (NIH Publication No. 85–23, revised 1985). In addition, the Department of Zoology, Faculty of Science, Helwan University (Cairo, Egypt) has approved the experimental protocol and animal handling (Authorize Number: HU2019/Z/AER0219-011).

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kassab, R.B., Elbaz, M., Oyouni, A.A.A. et al. Anticolitic activity of prodigiosin loaded with selenium nanoparticles on acetic acid–induced colitis in rats. Environ Sci Pollut Res 29, 55790–55802 (2022). https://doi.org/10.1007/s11356-022-19747-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-19747-1

Keywords

Search

Navigation