Sains Malaysiana 47(7)(2018): 1393–1400

http://dx.doi.org/10.17576/jsm-2018-4707-06

Heavy Metals Content in Paraphilometroides nemipteri from South China Sea may Influence Level of Glutathione and P38 Protein Expression

(Kandungan Logam Berat dalam Paraphilometroides nemipteri dari Laut China Selatan

Boleh Mempengaruhi Tahap Glutation dan Ekspresi Protein P38)

NURUL HUDA ABD KADIR^1,3*, MOHD FAUZI MAHMUD¹, MOHAMAD KHAIRI MOHD ZAINOL², MASTURA ABD MALEK^3,5 & FAIZAH SHAHAROM HARRISON^3,4

¹School of Fundamental Science, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu Darul Iman, Malaysia

²School of Science and Food Technology, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu Darul Iman, Malaysia

³Institute of Tropical Aquaculture (AQUATROP), Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu Darul Iman, Malaysia

⁴School of Fisheries and Aquaculture, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu Darul Iman, Malaysia

⁵Institute of Medical Molecular Biotechnoloy (IMMB), Faculty of Medicine, Universiti Teknologi MARA, Selangor Branch, Sungai Buloh Campus, 47000 Sungai Buloh, Selangor Darul Ehsan, Malaysia

Diserahkan: 21 November 2017/Diterima: 19 Februari 2018

ABSTRACT

Numerous studies have shown that parasites potentially become bio-accumulators for heavy metals. The heavy metals content in parasite-infected fish was reported to be lower compared to the parasite non-infected fish. Evaluation of heavy metal content in Nemipterus peronii and Paraphilometroides nemipteri was performed using ICP-OES. Our result has shown that arsenic was the most abundance heavy metal content in muscle N. peronii and P. nemipteri, suggesting that the parasite has the ability to accumulate heavy metals. Heavy metals were reported to induce oxidative stress where glutathione and p38 protein may be involved. Thus, expression of the p38 protein was determined using western blot technique and glutathione content was measured fluorometrically. The p38 expression in P. nemipteri of Pulau Kambing was higher compared to P. nemipteri of Besut has shown that the parasite may exposed to stress. Glutathione content showed no significant changes due to detoxification mechanism occurred in the parasite. In this study, we could conclude that P. nemipteri could be a bio-accumulator, whereas p38 protein and glutathione as indicator of stress level in the parasite that exposed to the heavy metals.

Keywords: Glutathione; heavy metals, Nemipterus peronii; oxidative stress; Paraphilometroides nemipterii

ABSTRAK

Banyak kajian telah menunjukkan bahawa parasit berpotensi menjadi bio-akumulator bagi logam berat. Kandungan logam berat dalam ikan yang dijangkiti parasit dilaporkan lebih rendah berbanding ikan parasit yang tidak dijangkiti parasit. Penilaian kandungan logam berat dalam Nemipterus peronii dan Paraphilometroides nemipteri dilakukan menggunakan ICP-OES. Keputusan yang diperoleh menunjukkan bahawa arsenik merupakan kandungan logam berat yang paling banyak di dalam otot N. peronii dan P. nemipteri, ini menunjukkan bahawa parasit mempunyai keupayaan untuk mengumpul logam berat. Logam berat dilaporkan menyebabkan tekanan oksidatif dengan protein glutation dan p38 mungkin terlibat. Oleh itu, ekspresi protein p38 ditentukan dengan menggunakan teknik Western blot dan kandungan glutation diukur secara fluorometri. Ekspresi protein p38 oleh P. nemipteri dari Pulau Kambing adalah lebih tinggi berbanding P. nemipteri di Besut, menunjukkan bahawa parasit mungkin terdedah kepada tekanan. Kandungan glutation tidak menunjukkan perubahan ketara disebabkan oleh mekanisme detoksifikasi yang berlaku pada parasit. Dalam kajian ini, kita dapat menyimpulkan bahawa P. nemipteri boleh menjadi bio-akumulator melalui ekspresi protein p38 dan glutation sebagai penunjuk aras tekanan dalam parasit yang terdedah kepada logam berat.

Kata kunci: Glutation; logam berat; Nemipterus peronii; Paraphilometroides nemipterii; tekanan oksidatif

RUJUKAN

Allen, T., Singhal, R. & Rana, S.V.S. 2004. Resistance to oxidative stress in a freshwater fish Channa punctatus after exposure to inorganic arsenic. Biological Trace Element Research 98(1): 63-72.

Ambak, M.A., Isa, M.M., Zakaria, M.Z. & Ghaffar, M.A. 2012. Fishes of Malaysia. Terengganu: Penerbit UMT.

Bagal-Kestwal, D., Karve, M.S., Kakade, B. & Pillai, V.K. 2008. Invertase inhibition based electrochemical sensor for the detection of heavy metal ions in aqueous system: Application of ultra-microelectrode to enhance sucrose biosensor’s sensitivity. Biosensors and Bioelectronics 24(4): 657-664.

Bhattacharya, A. & Bhattacharya, S. 2007. Induction of oxidative stress by arsenic in Clarias batrachus: Involvement of peroxisomes. Ecotoxicology and Environmental Safety 66(2): 178-187.

Blackwell, T.K., Steinbaugh, M.J., Hourihan, J.M., Ewald, C.Y. & Isik, M. 2015. SKN-1/Nrf, stress responses, and aging in Caenorhabditis elegans. Free Radical Biology and Medicine 88(Part B): 290-301.

Brázová, T., Torres, J., Eira, C., Hanzelová, V., Miklisová, D. & Šalamún, P. 2012. Perch and its parasites as heavy metal biomonitors in a freshwater environment: The case study of the Ružín Water Reservoir, Slovakia. Sensors 12(3): 3068-3081.

Canesi, L., Viarengo, A., Leonzio, C., Filippelli, M. & Gallo, G. 1999. Heavy metals and glutathione metabolism in mussel tissues. Aquatic Toxicology 46(1): 67-76.

Chee, P.S., Suhaimi, S., Keat, C.C., Noor, A.M.S. & Norhayati, M.T. 2008. Metal geochemistry of Nerus River, Terengganu. Malaysian Journal of Analytical Sciences 12(3): 593-599.

Elia, A.C., Galarini, R., Taticchi, M.I., Dörr, A.J.M. & Mantilacci, L. 2003. Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicology and Environmental Safety 55(2): 162-167.

Ercal, N., Gurer-Orhan, H. & Aykin-Burns, N. 2001. Toxic metals and oxidative stress Part I: Mechanisms involved in metal-induced oxidative damage. Current Topics in Medicinal Chemistry 1(6): 529-539.

Espinoza, H.M., Williams, C.R. & Gallagher, E.P. 2012. Effect of cadmium on glutathione S-transferase and metallothionein gene expression in coho salmon liver, gill and olfactory tissues. Aquatic Toxicology 110: 37-44.

Farombi, E., Adelowo, O. & Ajimoko, Y. 2007. Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun River. International Journal of Environmental Research and Public Health 4(2): 158- 165.

Gümgüm, B., ünlü, E., Tez, Z. & Gülsün, Z. 1994. Heavy metal pollution in water, sediment and fish from the Tigris River in Turkey. Chemosphere 29(1): 111-116.

Hassan, A.H., Al-Zanbagi, N.A. & Al-Nabati, E.A. 2016. Impact of nematode helminthes on metal concentrations in the muscles of Koshar fish, Epinephelus summana, in Jeddah, Saudi Arabia. The Journal of Basic & Applied Zoology 74: 56-61.

Hayes, J.D. & Strange, R.C. 2000. Glutathione S-Transferase polymorphisms and their biological consequences. Pharmacology 61(3): 154-166.

Helmcke, K.J. & Aschner, M. 2010. Hormetic effect of methylmercury on Caenorhabditis elegans. Toxicology and Applied Pharmacology 248(2): 156-164.

Jarić, I., Višnjić-Jeftić, Ž., Cvijanović, G., Gačić, Z., Jovanović, L., Skorić, S. & Lenhardt, M. 2011. Determination of differential heavy metal and trace element accumulation in liver, gills, intestine and muscle of sterlet (Acipenser ruthenus) from the Danube River in Serbia by ICP-OES. Microchemical Journal 98(1): 77-81.

Johnson, G.L. & Lapadat, R. 2002. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science 298(5600): 1911-1912.

Kamaruzzaman, B., Rina, Z., John, B.A. & Jalal, K. 2011. Heavy metal accumulation in commercially important fishes of South West Malaysian coast. Research Journal of Environmental Sciences 5(6): 595-602.

Karadede, H. & Ünlü, E. 2000. Concentrations of some heavy metals in water, sediment and fish species from the Atatürk  Dam Lake (Euphrates), Turkey. Chemosphere 41(9): 1371- 1376.

Kim, S.D., Moon, C.K., Eun, S.Y., Ryu, P.D. & Jo, S.A. 2005. Identification of ASK1, MKK4, JNK, c-Jun, and caspase-3 as a signaling cascade involved in cadmium-induced neuronal cell apoptosis. Biochemical and Biophysical Research Communications 328(1): 326-334.

Kumar, B., Sajwan, K. & Mukherjee, D. 2012. Distribution of heavy metals in valuable coastal fishes from North East Coast of India. Turkish Journal of Fisheries and Aquatic Sciences 12(1): 81-88.

Labuda, J., Bubnicova, K.K., Kovalova, L., Vanickova, M., Mattusch, J. & Wennrich, R. 2005. Voltammetric detection of damage to DNA by arsenic compounds at a DNA biosensor. Sensors 5(6): 411-423.

Lee, Y.H. & Stuebing, R.B. 1990. Heavy metal contamination in the River Toad, Bufo juxtasper (Inger), near a copper mine in East Malaysia. Bulletin of Environmental Contamination and Toxicology 45(2): 272-279.

Liao, V.H. & Yu, C.W. 2005. Caenorhabditis elegans gcs-1 confers resistance to arsenic-induced oxidative stress. Biometals 18(5): 519-528.

Mazhar, R., Shazili, N.A. & Harrison, F.S. 2014. Comparative study of the metal accumulation in Hysterothalycium reliquens (nematode) and Paraphilometroides nemipteri (nematode) as compared with their doubly infected host, Nemipterus peronii (Notched threadfin bream). Parasitology Research 113(10): 3737-3743.

Nishida, Y. 2011. The chemical process of oxidative stress by copper(II) and iron(III) ions in several neurodegenerative disorders. Monatshefte für Chemie - Chemical Monthly 142(4): 375-384.

Palaniappan, P.R. & Karthikeyan, S. 2009. Bioaccumulation and depuration of chromium in the selected organs and whole body tissues of freshwater fish Cirrhinus mrigala individually and in binary solutions with nickel. Journal of Environmental Sciences 21(2): 229-236.

Rana, A., Gallo, K., Godowski, P., Hirai, S.I., Ohno, S., Zon, L., Kyriakis, J.M. & Avruch, J. 1996. The mixed lineage kinase SPRK phosphorylates and activates the stress-activated protein kinase activator, SEK-1. Journal of Biological Chemistry 271(32): 19025-19028.

Rejomon, G., Nair, M. & Joseph, T. 2010. Trace metal dynamics in fishes from the southwest coast of India. Environmental Monitoring and Assessment 167(1): 243-255.

Ressurreição, M., Rollinson, D., Emery, A.M. & Walker, A.J. 2011. A role for p38 mitogen-activated protein kinase in early post-embryonic development of Schistosoma mansoni. Molecular and Biochemical Parasitology 180(1): 51-55.

Rios-Barrera, D., Vega-Segura, A., Thibert, V., Rodríguez-Zavala, J.S. & Torres-Marquez, M.E. 2008. p38 MAPK as a signal transduction component of heavy metals stress in Euglena gracilis. Archives of Microbiology 191(1): 47-54.

Sahu, S.N., Lewis, J., Patel, I., Bozdag, S., Lee, J.H., Sprando, R. & Cinar, H.N. 2013. Genomic analysis of stress response against arsenic in Caenorhabditis elegans. PLOS ONE 8(7): e66431.

Saliu, J.K. & Bawa-Allah, K.A. 2012. Toxicological effects of lead and zinc on the antioxidant enzyme activities of post juvenile Clarias gariepinus. Resources and Environment 2(1): 21-26.

Sevcikova, M., Modra, H., Slaninova, A. & Svobodova, Z. 2011. Metals as a cause of oxidative stress in fish: A review. Vet. Med. 56(11): 537-546.

Stohs, S.J. & Bagchi, D. 1995. Oxidative mechanisms in the toxicity of metal ions. Free Radical Biology and Medicine 18(2): 321-336.

Suratman, S., Tahir, N.M., Yeow, L.C. & Rashid, S.R.A. 2006. Kesan monsun terhadap kualiti air di Lembangan Sungai Besut, Terengganu. Malaysian Journal of Analytical Sciences 10(1): 143-148.

Sures, B., Siddall, R. & Taraschewski, H. 1999. Parasites as accumulation indicators of heavy metal pollution. Parasitology Today 15(1): 16-21.

Tekaya, N., Saiapina, O., Ben Ouada, H., Lagarde, F., Ben Ouada, H. & Jaffrezic-Renault, N. 2013. Ultra-sensitive conductometric detection of heavy metals based on inhibition of alkaline phosphatase activity from Arthrospira platensis. Bioelectrochemistry 90: 24-29.

Valko, M., Morris, H. & Cronin, M. 2005. Metals, toxicity and oxidative stress. Current Medicinal Chemistry 12(10): 1161-1208.

Ventura-Lima, J., Bogo, M.R. & Monserrat, J.M. 2011. Arsenic toxicity in mammals and aquatic animals: A comparative biochemical approach. Ecotoxicology and Environmental Safety 74(3): 211-218.

Wang, S., Tang, M., Pei, B., Xiao, X., Wang, J., Hang, H. & Wu, L. 2008. Cadmium-induced germline apoptosis in Caenorhabditis elegans: The roles of HUS1, p53, and MAPK signaling pathways. Toxicological Sciences 102(2): 345-351.

Wilhelm, D., Bender, K., Knebel, A. & Angel, P. 1997. The level of intracellular glutathione is a key regulator for the induction of stress-activated signal transduction pathways including Jun N-terminal protein kinases and p38 kinase by alkylating agents. Molecular and Cellular Biology 17(8): 4792-800.

Zimmermann, S., Sures, B. & Taraschewski, H. 1999. Experimental studies on lead accumulation in the eel-specific endoparasites Anguillicola crassus (Nematoda) and Paratenuisentis ambiguus (Acanthocephala) as compared with their host, Anguilla anguilla. Archives of Environmental Contamination and Toxicology 37(2): 190-195.

*Pengarang untuk surat-menyurat: nurulhuda@umt.edu.my