Promising Chemoprevention of Colonic Aberrant Crypt Foci by Portunus segnis Muscle and Shell Extracts in Azoxymethane-Induced Colorectal Cancer in Rats

Page: [2041 - 2052] Pages: 12

  • * (Excluding Mailing and Handling)

Abstract

Background and Purpose: This study subjected a rat model to the extracts of muscle and shell tissues from Portunus segnis to assess their therapeutic effects on the HT-29 colon cancer cells as well as on colonic Aberrant Crypt Foci (ACF) induced by Azoxymethane (AOM).

Methods: The cell line was exposed to the extracts to compare the cytotoxicity of hexane, butanol, ethyl acetate, and water extract of muscle and ethanolic extract of the shell. Male rats (n=40) were assigned into control, positive, negative, and treatment groups. The animals were injected with AOM, except the control group, and then exposed to 250 and 500mg/kg of the crude extracts. Immunohistochemical localization of Bax and Bcl-2, as well as ACF and antioxidant enzymes, were evaluated in the rat colon.

Results: The butanolic muscle extract and ethanolic shell one demonstrated an IC50 of 9.02±0.19μg/ml and 20.23±0.27μg/ml towards the cell line, respectively. Dietary exposure inhibited the ACF formation and crypt multiplicity in the colon compared to the cancer control group. The activity of SOD and CAT increased, while that of MDA decreased. The expression of Bax and Bcl-2 increased and decreased, respectively.

Conclusion: Taken together, the results show that both extractions were suggested to be suppressive to AOMinduced colon cancer.

Keywords: Portunus segnis, muscle, shell, colon cancer, azoxymethane, HT-29.

Graphical Abstract

[1]
Hendifar, A.; Yang, D.; Lenz, F.; Lurje, G.; Pohl, A.; Lenz, C.; Ning, Y.; Zhang, W.; Lenz, H-J. Gender disparities in metastatic colorectal cancer survival. Clin. Cancer Res., 2009, 15(20), 6391-6397.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-0877]
[2]
Jia, Y.; Guo, M. Epigenetic changes in colorectal cancer. Chin. J. Cancer, 2013, 32(1), 21.
[http://dx.doi.org/10.5732/cjc.011.10245]
[3]
Parkin, D.M.; Boyd, L.; Walker, L.C. The fraction of cancer attributable to lifestyle and environmental factors in the UK in 2010. Summary and Conclusions. Br. J. Cancer, 2011, 105(Suppl. 2), S77.
[http://dx.doi.org/10.1038/bjc.2011.489]
[4]
Danese, S.; Mantovani, A. Inflammatory bowel disease and intestinal cancer: A paradigm of the yin-yang interplay between inflammation and cancer. Oncogene, 2010, 29(23), 3313.
[http://dx.doi.org/10.1038/onc.2010.109]
[5]
Haggar, F.A.; Boushey, R.P. Colorectal cancer epidemiology: Incidence, mortality, survival, and risk factors. Clin. Colon Rectal Surg., 2009, 22(04), 191-197.
[http://dx.doi.org/10.1055/s-0029-1242458]
[6]
Rajendiran, V.; Natarajan, V.; Devaraj, S.N. Anti-inflammatory activity of Alpinia officinarum hance on rat colon inflammation and tissue damage in DSS induced acute and chronic colitis models. Food Sci. Hum. Wellness, 2018, 7(4), 273-281.
[http://dx.doi.org/10.1016/j.fshw.2018.10.004]
[7]
Sivaperumal, P.; Kamala, K.; Natarajan, E.; Dilipan, E. Antimicrobial peptide from crab haemolymph of Ocypoda macrocera (Maline Edwards 1852) with reference to antioxidant: A case study. Int. J. Pharm. Pharm. Sci., 2013, 5(Suppl. 2), S719-S727.
[8]
Rezakhani, L.; Rashidi, Z.; Mirzapur, P.; Khazaei, M. Antiproliferatory effects of crab shell extract on breast cancer cell line (MCF7). J. Breast Cancer, 2014, 17(3), 219-225.
[http://dx.doi.org/10.4048/jbc.2014.17.3.219]
[9]
Domard, A.; Domard, M. Chitosan: Structure-properties relationship and biomedical applications. Polym. Biomater., 2001, 2, 187-212.
[10]
Ghandour, A.M. Health hazards in humans and animals caused by imported livestock diseases in Saudi Arabia. Fauna Saudi Arab., 1988, 9, 468-477.
[11]
Büttiker, W.; Krupp, F. Fauna of Arabia; National Commission for Wildlife Conservation and Development: Saudi Arabia, 1993, Vol. 13, .
[12]
Hamdi, M.; Hammami, A.; Hajji, S.; Jridi, M.; Nasri, M.; Nasri, R. Chitin extraction from blue crab (Portunus segnis) and shrimp (Penaeus kerathurus) shells using digestive alkaline proteases from P. segnis Viscera. Int. J. Biol. Macromol., 2017, 101, 455-463.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.02.103]
[13]
Ayas, D. The chemical composition of sexually mature blue swimmer crab (Portunus pelagicus, Linnaeus 1758) in the Mersin bay. J. Fish., 2011, 33(3), 179-184.
[http://dx.doi.org/10.3153/jfscom.2011035]
[14]
Anjugam, M.; Iswarya, A. Antibiofilm competency of Portunus pelagicus haemolymph and identification of its bioactive compounds. J. Aquac. Res. Dev., 2016, 07(08)
[http://dx.doi.org/10.4172/2155-9546.1000444]
[15]
Priya, E.R.; Ravichandran, S.; Jawaharlal, P. Antimicrobial and antioxidant proteins from the Crab, Liagore rubromaculata (de Haan, 1835). World J. Pharm. Pharm. Sci., 2014, 3(10), 533-541.
[16]
Lekshmi, N.; Viveka, S.; Anusha, S.; Jeeva, S.; Brindha, R.; Selva Bharath, M. Antibacterial activity of fresh water crab and snail and isolation of antibacterial peptides from haemolymph by SDS-PAGE. Int. J. Pharm. Pharm. Sci., 2015, 7(1), 109-114.
[17]
Nisha, G. Antibacterial effect of crab shell extract against human pathogenic bacteria. Int. J. Sci. Eng. Tech. Res., 2015, 7, 5790-5791.
[18]
Laith, A.A.; Ambak, M.; Abol-Munafi, A.B.; Nurhafizah, W.W.I.; Najiah, M. Metabolomic analysis of marine and mud crabs based on antibacterial activity. Aquacult. Rep., 2017, 7, 7-15.
[http://dx.doi.org/10.1016/j.aqrep.2017.05.002]
[19]
Soundarapandian, P.V.D. Antibacterial activity of crab shell extracts against human pathogenic bacteria and usage of new drugs. J. Dev. Drugs, 2013, 02(02), 10-12.
[http://dx.doi.org/10.4172/2329-6631.1000110]
[20]
Veeruraj, A.; Ravichandran, S.; Rameshkumar, G. Antibacterial activity of crab haemolymph on clinical pathogens. Trends Appl. Sci. Res., 2008, 3(2), 174-181.
[http://dx.doi.org/10.3923/tasr.2008.174.181]
[21]
Bejaoui, S.; Ghribi, F.; Hatira, S.; Chetoui, I.; Rebah, I.; El Cafsi, M. First investigation in the biochemical analysis of the invasive crab Portunus segnis from Tunisian waters. J. Am. Oil Chem. Soc., 2017, 94(5), 673-682.
[http://dx.doi.org/10.1007/s11746-017-2987-x]
[22]
Wu, X.; Zhou, B.; Cheng, Y.; Zeng, C.; Wang, C.; Feng, L. Comparison of gender differences in biochemical composition and nutritional value of various edible parts of the Blue Swimmer Crab. J. Food Compos. Anal., 2010, 23(2), 154-159.
[http://dx.doi.org/10.1016/j.jfca.2009.08.007]
[23]
Chaiyawat, M.; Eungrasamee, I.; Raksakulthai, N. Quality characteristics of Blue Swimming Crab (Portunus pelagicus, Linnaeus 1758) meat fed Gracilaria edulis (Gmelin) silva. Witthayasan Kasetsat Witthayasat, 2008, 42, 522-530.
[24]
Hamdi, M.; Nasri, R.; Dridi, N.; Li, S.; Nasri, M. Development of novel high-selective extraction approach of carotenoproteins from Blue Crab (Portunus segnis) shells, contribution to the qualitative analysis of bioactive compounds by HR-ESI-MS. Food Chem., 2020, 302125334
[25]
Jiang, W.; Liu, Y.; Yang, X.; Hu, S. Antioxidant and antibacterial activities of modified crab shell bioactive peptides by Maillard reaction. Int. J. Food Prop., 2018, 21(1), 2730-2743.
[http://dx.doi.org/10.1080/10942912.2018.1561463]
[26]
Marotta, F.; Naito, Y.; Minelli, E.; Tajiri, H.; Bertuccelli, J.; Wu, C.C.; Min, C.H.; Hotten, P.; Fesce, E. Chemopreventive effect of a probiotic preparation on the development of preneoplastic and neoplastic colonic lesions: An experimental study. Hepatogastroenterology, 2002, 50(54), 1914-1918.
[27]
Nordlinger, B.; Panis, Y.; Puts, J.P.; Herve, J.P.; Delelo, R.; Ballet, F. Experimental model of colon cancer: Recurrences after surgery alone or associated with intraperitoneal 5-fluorouracil chemotherapy. Dis. Colon Rectum, 1991, 34(8), 658-663.
[http://dx.doi.org/10.1007/BF02050346]
[28]
Council, N.R. Guide for the Care and Use of Laboratory Animals; National Academies Press, 2010.
[29]
Weatheall, D. A Working group report chaired by Sir David Weatheall FRS FMedSci.The Use of Non-Human Primates in Research,, 2006, 147
[30]
Salga, M.S.; Ali, H.M.; Abdulla, M.A.; Abdelwahab, S.I. Gastroprotective activity and mechanism of novel dichlorido-zinc (II)-4-(2-(5-methoxybenzylideneamino) ethyl) piperazin-1-iumphenolate complex on ethanol-induced gastric ulceration. Chem. Biol. Interact., 2012, 195(2), 144-153.
[http://dx.doi.org/10.1016/j.cbi.2011.11.008]
[31]
Pearson, L.; Mihali, T.; Moffitt, M.; Kellmann, R.; Neilan, B. On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Mar. Drugs, 2010, 8(5), 1650-1680.
[http://dx.doi.org/10.3390/md8051650]
[32]
Karan, T.; Erenler, R. Fatty acid constituents and anticancer activity of Cladophora fracta (Of Müller Ex Vahl) Kützing. Trop. J. Pharm. Res., 2018, 17(10), 1977-1982.
[http://dx.doi.org/10.4314/tjpr.v17i10.12]
[33]
Ukwubile, C.A.; Ahmed, A.; Katsayal, U.A.; Ya’u, J.; Mejida, S. GC-MS analysis of bioactive compounds from Melastomastrum capitatum (Vahl)Fern. leaf methanol extract: An anticancer plant. Sci. African, 2019, 3, 10-17.
[http://dx.doi.org/10.1016/j.sciaf.2019.e00059]
[34]
Yu, F-R.; Lian, X-Z.; Guo, H-Y.; McGuire, P.M.; Li, R-D.; Wang, R.; Yu, F-H. Isolation and characterization of methyl esters and derivatives from Euphorbia kansui (Euphorbiaceae) and their inhibitory effects on the human SGC-7901 cells. J. Pharm. Pharm. Sci., 2005, 8(3), 528-535.
[35]
Mishra, S.; Verma, S.S.; Rai, V.; Awasthee, N.; Arya, J.S.; Maiti, K.K.; Gupta, S.C. Curcuma raktakanda induces apoptosis and suppresses migration in cancer cells: Role of reactive oxygen species. Biomolecules, 2019, 9(4)
[http://dx.doi.org/10.3390/biom9040159]
[36]
Combs, G.F., Jr; Gray, W.P. Chemopreventive agents. Selenium. Pharmacol. Ther., 1998, 79(3), 179-192.
[http://dx.doi.org/10.1016/S0163-7258(98)00014-X]
[37]
Mirzapur, P.; Rashidi, Z.; Rezakhani, L.; Khazaei, M. In vitro inhibitory effect of crab shell extract on human umbilical vein endothelial cell. Vitr. Cell. Dev. Biol. Anim., 2015, 51(1), 36-41.
[http://dx.doi.org/10.1007/s11626-014-9810-x]
[38]
Ip, C.; Dong, Y. Methylselenocysteine modulates proliferation and apoptosis biomarkers in premalignant lesions of the rat mammary gland. Anticancer Res., 2001, 21(2A), 863-867.
[39]
Ip, C.; Dong, Y.; Ganther, H.E. New concepts in selenium chemoprevention. Cancer Metastasis Rev., 2002, 21(3-4), 281-289.
[http://dx.doi.org/10.1023/A:1021263027659]
[40]
Suzuki, M.; Endo, M.; Shinohara, F.; Echigo, S.; Rikiishi, H. Differential apoptotic response of human cancer cells to organoselenium compounds. Cancer Chemother. Pharmacol., 2010, 66(3), 475-484.
[http://dx.doi.org/10.1007/s00280-009-1183-6]
[41]
Brozmanová, J.; Mániková, D.; Vlčková, V.; Chovanec, M. Selenium: A double-edged sword for defense and offence in cancer. Arch. Toxicol., 2010, 84(12), 919-938.
[http://dx.doi.org/10.1007/s00204-010-0595-8]
[42]
Hamdi, M.; Hajji, S.; Affes, S.; Taktak, W.; Maâlej, H.; Nasri, M.; Nasri, R. Development of a controlled bioconversion process for the recovery of chitosan from Blue Crab (Portunus segnis). Exoskeleton. Food Hydrocoll., 2018, 77, 534-548.
[http://dx.doi.org/10.1016/j.foodhyd.2017.10.031]
[43]
Scheers, E.M.; Ekwall, B.; Dierickx, P.J. In vitro long-term cytotoxicity testing of 27 MEIC chemicals on Hep G2 cells and comparison with acute human toxicity data. Toxicol. Vitr., 2001, 15(2), 153-161.
[http://dx.doi.org/10.1016/S0887-2333(00)00062-X]
[44]
Clemedson, C.; Ekwall, B. Overview of the final MEIC results: The in vitro--in vitro evaluation. Toxicol. Vitr., 1999, 13(4-5), 657-663.
[http://dx.doi.org/10.1016/S0887-2333(99)00060-0]
[45]
Mehdi, S.J.; Ahmad, A.; Irshad, M.; Manzoor, N.; Rizvi, M.M.A. Cytotoxic effect of carvacrol on human cervical cancer cells. Biol. Med. (Aligarh), 2011, 3(2), 307-312.
[46]
Choi, E.J.; Lee, J.I.; Kim, G-H. Evaluation of the anticancer activities of thioflavanone and thioflavone in human breast cancer cell lines. Int. J. Mol. Med., 2012, 29(2), 252-256.
[47]
Perego, S.; Cosentino, S.; Fiorilli, A.; Tettamanti, G.; Ferraretto, A. Casein phosphopeptides modulate proliferation and apoptosis in HT-29 cell line through their interaction with voltage-operated L-Type calcium channels. J. Nutr. Biochem., 2012, 23(7), 808-816.
[http://dx.doi.org/10.1016/j.jnutbio.2011.04.004]
[48]
Takayama, T.; Katsuki, S.; Takahashi, Y.; Ohi, M.; Nojiri, S.; Sakamaki, S.; Kato, J.; Kogawa, K.; Miyake, H.; Niitsu, Y. Aberrant Crypt Foci of the colon as precursors of adenoma and cancer. N. Engl. J. Med., 1998, 339(18), 1277-1284.
[http://dx.doi.org/10.1056/NEJM199810293391803]
[49]
Velmurugan, B.; Singh, R.P.; Agarwal, R.; Agarwal, C. Dietary‐feeding of grape seed extract prevents azoxymethane‐induced colonic aberrant Crypt Foci formation in fischer 344 rats. Mol. Carcinog., 2010, 49(7), 641-652.
[http://dx.doi.org/10.1002/mc.20643]
[50]
Kawamori, T.; Tanaka, T.; Hirose, Y.; Ohnishi, M.; Mori, H. Inhibitory effects of D-Limonene on the development of colonic aberrant Crypt Foci induced by azoxymethane in F344 rats. Carcinogenesis, 1996, 17(2), 369-372.
[http://dx.doi.org/10.1093/carcin/17.2.369]
[51]
Esmaeelian, B.; Benkendorff, K.; Le Leu, R.K.; Abbott, C.A. Simultaneous assessment of the efficacy and toxicity of marine mollusk-derived brominated indoles in an in vivo model for early stage colon cancer. Integr. Cancer Ther., 2018, 17(2), 248-262.
[http://dx.doi.org/10.1177/1534735417699880]
[52]
Al-Henhena, N.; Khalifa, S.A.M.; Ying, R.P.Y.; Ismail, S.; Hamadi, R.; Shawter, A.N.; Idris, A.M.; Azizan, A.; Al-Wajeeh, N.S.; Abdulla, M.A. Evaluation of chemopreventive potential of strobilanthes crispus against colon cancer formation in vitro and in vivo. BMC Complement. Altern. Med., 2015, 15(1), 1-11.
[http://dx.doi.org/10.1186/s12906-015-0926-7]
[53]
Waly, M.I.; Al-Rawahi, A.S.; Al Riyami, M.; Al-Kindi, M.A.; Al-Issaei, H.K.; Farooq, S.A.; Al-Alawi, A.; Rahman, M.S. Amelioration of azoxymethane induced-carcinogenesis by reducing oxidative stress in rat colon by natural extracts. BMC Complement. Altern. Med., 2014, 14
[http://dx.doi.org/10.1186/1472-6882-14-60]]
[54]
Xiao, Y.; Bi, C.; Fan, Y.; Cui, C.; Zhang, X.; Dou, Q.P. L-glutamine schiff base copper complex as a proteasome inhibitor and an apoptosis inducer in human cancer cells. Int. J. Oncol., 2008, 33(5), 1073-1079.
[55]
Reuter, S.; Gupta, S.C.; Chaturvedi, M.M.; Aggarwal, B.B. Oxidative stress, inflammation, and cancer: How are they linked? Free Radic. Biol. Med., 2010, 49(11), 1603-1616.
[http://dx.doi.org/10.1016/j.freeradbiomed.2010.09.006]
[56]
Watson, J.L.; Hill, R.; Yaffe, P.B.; Greenshields, A.; Walsh, M.; Lee, P.W.; Giacomantonio, C.A.; Hoskin, D.W. Curcumin causes superoxide anion production and P53-independent apoptosis in human colon cancer cells. Cancer Lett., 2010, 297(1), 1-8.
[http://dx.doi.org/10.1016/j.canlet.2010.04.018]
[57]
Moghadamtousi, S.Z.; Rouhollahi, E.; Karimian, H.; Fadaeinasab, M.; Firoozinia, M.; Abdulla, M.A.; Kadir, H.A. The chemopotential effect of Annona muricata leaves against azoxymethane-induced colonic aberrant Crypt Foci in rats and the apoptotic effect of acetogenin annomuricin E in HT-29 cells: A bioassay-guided approach. PLoS One, 2015, 10(4)e0122288
[http://dx.doi.org/10.1371/journal.pone.0122288]]
[58]
Al-Numair, K.S.; Waly, M.I.; Ali, A.; Essa, M.M.; Farhat, M.F.; Alsaif, M.A. Dietary folate protects against azoxymethane-induced aberrant Crypt Foci development and oxidative stress in rat colon. Exp. Biol. Med. (Maywood), 2011, 236(9), 1005-1011.
[http://dx.doi.org/10.1258/ebm.2011.011010]
[59]
Rodríguez‐Ramiro, I.; Ramos, S.; López‐Oliva, E.; Agis-Torres, A.; Gómez-Juaristi, M.; Mateos, R.; Bravo, L.; Goya, L.; Martín, M.Á. Cocoa-rich diet prevents azoxymethane‐induced colonic preneoplastic lesions in rats by restraining oxidative stress and cell proliferation and inducing apoptosis. Mol. Nutr. Food Res., 2011, 55(12), 1895-1899.
[http://dx.doi.org/10.1002/mnfr.201100363]
[60]
Rasool, N.; Rizwan, K.; Zubair, M.; Naveed, K.U.R.; Imran, I.; Ahmed, V.U. Antioxidant potential of different extracts and fractions of Catharanthus roseus shoots. Int. J. Phytomedicine, 2011, 3(1), 108.
[61]
Hajrezaie, M.; Paydar, M.; Looi, C.Y.; Moghadamtousi, S.Z.; Hassandarvish, P.; Salga, M.S.; Karimian, H.; Shams, K.; Zahedifard, M.; Majid, N.A. Apoptotic effect of novel schiff based CdCl2 (C14H21N3O2) complex is mediated via activation of the mitochondrial pathway in colon cancer cells. Sci. Rep., 2015, 5, 9097.
[http://dx.doi.org/10.1038/srep09097]
[62]
Hajrezaie, M.; Shams, K.; Moghadamtousi, S.Z.; Karimian, H.; Hassandarvish, P.; Emtyazjoo, M.; Zahedifard, M.; Majid, N.A.; Ali, H.M.; Abdulla, M.A. Chemoprevention of colonic aberrant Crypt Foci by novel schiff based dichlorido (4-methoxy-2-[2-(piperazin-4-Ium-1-Yl) ethyl] iminomethyl phenolate) Cd complex in azoxymethane-induced colorectal cancer in rats. Sci. Rep., 2015, 5, 12379.
[http://dx.doi.org/10.1038/srep12379]
[63]
Rao, C.V.; Simi, B.; Reddy, B.S. Inhibition by dietary curcumin of azoxymethane-induced ornithine decarboxylase, tyrosine protein kinase, arachidonic acid metabolism and aberrant Crypt Foci formation in the rat colon. Carcinogenesis, 1993, 14(11), 2219-2225.
[http://dx.doi.org/10.1093/carcin/14.11.2219]]
[64]
Tanaka, T.; Kawabata, K.; Kakumoto, M.; Hara, A.; Murakami, A.; Kuki, W.; Takahashi, Y.; Yonei, H.; Maeda, M.; Ota, T. Citrus auraptene exerts dose-dependent chemopreventive activity in rat large bowel tumorigenesis: The inhibition correlates with suppression of cell proliferation and lipid peroxidation and with induction of phase II drug-metabolizing enzymes. Cancer Res., 1998, 58(12), 2550-2556.
[65]
Hernández-Muñoz, R.; Montiel-Ruíz, C.; Vázquez-Martínez, O. Gastric mucosal cell proliferation in ethanol-induced chronic mucosal injury is related to oxidative stress and lipid peroxidation in rats. Lab. Invest., 2000, 80(8), 1161.
[http://dx.doi.org/10.1038/labinvest.3780124]
[66]
Lee, W-R.; Shen, S-C.; Lin, H-Y.; Hou, W-C.; Yang, L-L.; Chen, Y-C. Wogonin and fisetin induce apoptosis in human promyeloleukemic cells, accompanied by a decrease of reactive oxygen species, and activation of caspase 3 and Ca2+-dependent endonuclease. Biochem. Pharmacol., 2002, 63(2), 225-236.
[http://dx.doi.org/10.1016/S0006-2952(01)00876-0]
[67]
Yang, H-L.; Chen, C-S.; Chang, W-H.; Lu, F-J.; Lai, Y-C.; Chen, C-C.; Hseu, T-H.; Kuo, C-T.; Hseu, Y-C. Growth inhibition and induction of apoptosis in MCF-7 breast cancer cells by Antrodia camphorata. Cancer Lett., 2006, 231(2), 215-227.
[http://dx.doi.org/10.1016/j.canlet.2005.02.004]
[68]
Bousserouel, S.; Gosse, F.; Bouhadjar, M.; Soler, L.; Marescaux, J.; Raul, F. Long-term administration of aspirin inhibits tumour formation and triggers anti-neoplastic molecular changes in a pre-clinical model of colon carcinogenesis. Oncol. Rep., 2010, 23(2), 511-517.