Advertisement

Cytotoxic effects of Tetraselmis suecica chloroform extracts with silver nanoparticle co-application on MCF-7, 4 T1, and Vero cell lines

  • Hanaa Ali Hussein
  • Habsah Mohamad
  • Maziah Mohd Ghazaly
  • A. A. Laith
  • Mohd Azmuddin AbdullahEmail author
Article

Abstract

In the present study we evaluated the effects of silver nanoparticles (AgNPs) and Tetraselmis suecica chloroform (CHL) crude extracts as single and co-applications against MCF-7 and 4 T1 breast cancer cells and normal Vero cell-lines. The AgNPs single application exhibited the highest cytotoxicity in a dose-dependent manner with IC50 of 5.3, 17.78, and 25.11 μg mL−1 against MCF-7, 4 T1 and Vero cell lines, respectively, after 72 h treatments. The AgNPs-T. suecica-CHL co-application at 2:1 ratio achieved the IC50 of 6.60 and 53.7 μg mL−1 on MCF-7 and 4 T1 cells, respectively, while the T. suecica-CHL single application only showed the IC50 of 46.77 and 83.17 μg mL−1, respectively. However, both the T. suecica-CHL and AgNPs-T. suecica-CHL showed no cytotoxic activity against the Vero cells. The AgNPs-T. suecica-CHL exhibited the highest late apoptotic events on MCF-7 (38.8%), followed by Tamoxifen (TMX), AgNPs and T. suecica-CHL. The cell cycle analysis of AgNPs-T. suecica-CHL–treated cells showed a significant increase in the accumulation of events at sub-G1 phase with increased ADP/ATP ratio and Caspase 3/7, suggesting the induction of apoptosis. The results brought new insights into the formulation of microalgal crude extracts (MCEs) and AgNPs co-applications in exerting strong cytotoxic effects on MCF-7 and 4 T1 cancer cells, but without having any cytotoxicity on the normal Vero cell-lines.

Keywords

Microalgae Natural product Chlorophyta Tetraselmis suecica Silver nanoparticles Co-application Anti-cancer agent 

Notes

Acknowledgments

The authors thank the Science Officers in the Institute of Marine Biotechnology, Universiti Malaysia Terengganu for their assistance with the facilities for the experiments, and Mr. Syed Ahmad Tajudin and Mr. Haziq Hamid from the Laboratory of Animal Cell Culture in Universiti Sultan Zainal Abidin, Tembila Campus, Besut, Terengganu, for their assistance in flow cytometric analyses.

Funding information

This research was funded by the Fundamental Research Grant Scheme (FRGS/1/2015/SG05/UMT/02/4) under the Ministry of Higher Education, Malaysia.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10811_2019_1905_MOESM1_ESM.docx (15 kb)
Table S1 Preparation of AgNPs-T. suecica-CHL ratio (DOCX 15 kb)

References

  1. Abdullah MA, Shah SMU, Shanab SMM, Ali HEA (2017) Integrated algal bioprocess engineering for enhanced productivity of lipid, carbohydrate and high-value bioactive compounds, Research and Review. J Microbiol Biotechnol 6:61–92Google Scholar
  2. Abdullah MA, Ahmad A, Shah SMS, Shanab SMM, Ali HEA, Abo-State MAM, Othman MF (2016) Integrated algal engineering for bioenergy generation, effluent remediation and production of high-value bioactive compounds. Biotechnol Bioprocess Eng 21:236–249CrossRefGoogle Scholar
  3. Abdullah MA, Shah SMU, Ahmad A, El-Sayed H (2015) Algal biotechnology for bioenergy, environmental remediation and high value biochemicals. In: Thangadurai D, Sangeetha J (eds) Biotechnology and Bioinformatics: Advances and Applications for Bioenergy, Bioremediation, and Biopharmaceutical Research. CRC Press / Apple Academic Press, New Jersey, USA, pp 301–344Google Scholar
  4. Abdullah MA, Gul-e-Saba AA, Abdah A (2014) Cytotoxic Effects of drug-loaded hyaluronan-glutaraldehyde cross-linked nanoparticles and the release kinetics modeling. J Adv Chem Eng 1:1000104Google Scholar
  5. Adhoni SA, Thimmappa SC, Kaliwal BB (2016) Phytochemical analysis and antimicrobial activity of Chlorella vulgaris isolated from Unkal Lake. J Coast Life Med 4:368–373CrossRefGoogle Scholar
  6. Al-saif SSA, Abdel-raouf N, El-Wazanani HA, Aref IA (2014) Antibacterial substances from marine algae isolated from Jeddah coast of Red Sea, Saudi Arabia. Saudi J Biol Sci 21:57–64CrossRefGoogle Scholar
  7. Alsufyani T (2014) Metabolite profiling of the chemosphere of the macroalga Ulva (Ulvales, Chlorophyta) and its associated bacteria. Dissertation. Thüringer Universitäts-und Landesbibliothek, JenaGoogle Scholar
  8. Andreotti K, Cree IA, Kurbacher M, Hartmann M, Linder D, Harel G, Gleiberman I, Caruso PA, Ricks SH, Untch M, Sartori C, Bruckner HW (1995) Chemosensitivity Testing of human tumors using a microplate adenosine triphosphate luminescence assay: clinical correlation for cisplatin resistance of ovarian carcinoma. Cancer Res 55:5276–5283Google Scholar
  9. AQUACOPs (1984) Review of ten years of experimental penaeid shrimp culture in Tahiti and New Caledonia (South Pacific). J World Maric Soc 15:73–91CrossRefGoogle Scholar
  10. Arokiyaraj S, Arasu MV, Vincent S, Prakash NU, Choi SH, Oh YK, Choi KC, Kim KH (2014) Rapid green synthesis of silver nanoparticles from Chrysanthemum indicum L and its antibacterial and cytotoxic effects: an in vitro study. Int J Nanomedicine 9:379–388CrossRefGoogle Scholar
  11. Arora S, Meena S (2018) Analysis of bioactive constituents from Ceropegia bulbosa Roxb. var. bulbosa: an endangered medicinal plant from Thar Desert of Rajasthan, India. J Pharmacogn Phytochem 7:2242–2247Google Scholar
  12. Atasever-arslan B, Yilancioglu K, Kalkan Z, Can A, Gür H, Isik FB, Deniz E, Erman B, Cetiner S (2016) Screening of new antileukemic agents from essential oils of algae extracts and computational modeling of their interactions with intracellular signaling nodes. Eur J Pharm Sci 83:120–131CrossRefGoogle Scholar
  13. Bai VDM, Krishnakumar S (2013) Evaluation of antimicrobial metabolites from marine microalgae Tetraselmis suecica using gas chromatography–mass spectrometry (GC–MS) analysis. Int J Pharm Pharm Sci 5:17–23Google Scholar
  14. Balamurugan M, Selvam GG, Thinakaran T, Sivakumar K (2014) Biochemical study and GC-MS analysis of Hypnea musciformis (Wulf.) Lamouroux. Am J Sci Res 8:117–123Google Scholar
  15. Borowitzka MA (1995) Microalgae as sources of pharmaceuticals and other biologically active compounds. J Appl Phycol 7:3–15CrossRefGoogle Scholar
  16. Bradbury DA, Simmons TD, Slater KJ, Crouch SPM (2000) Measurement of the ADP:ATP ratio in human leukaemic cell lines can be used as an indicator of cell viability, necrosis and apoptosis. J Immunol Methods 240:79–92CrossRefGoogle Scholar
  17. Cao KJ, Fan QY, Liu YL, Huang R, Yin CZ, Ma GS, Liu ZQ, Zeng YX (2008) Cancer incidence and mortality in Guangzhou City from 2000 to 2002. Chinese J Cancer 27:225–230Google Scholar
  18. Cohen GM (1997) Caspases: executioners of apoptosis. Biochem J 326:1–16CrossRefGoogle Scholar
  19. Cree IA, Pazzagli M, Mini E, Mazzei T, Hunter EM, Sutherland LA, Andreotti PE (1995) Methotrexate chemosensitivity by ATP luminescence in human leukemia cell lines and in breast cancer primary cultures: comparison of the TCA-100 assay with a clonogenic assay. Anti-Cancer Drugs 6:398–404CrossRefGoogle Scholar
  20. Crouch SPM, Kozlowski R, Slater K, Fletcher J (1993) The use of ATP bioluminescene as a measure of cell proliferation and cytotoxicity. J Immunol Methods 160:81–88CrossRefGoogle Scholar
  21. Curado MP (2011) Breast cancer in the world : incidence and mortality. Salud Publica Mex 53:372–384Google Scholar
  22. De La Mare JA, Lawson JC, Chiwakata MT, Beukes DR, Edkins AL, Blatch GL (2012) Quinones and halogenated monoterpenes of algal origin show anti-proliferative effects against breast cancer cells in vitro. Investig New Drugs 30:2187–2200CrossRefGoogle Scholar
  23. Devi JS, Bhimba BV (2012) Anticancer activity of silver nanoparticles synthesized by the seaweed Ulva lactuca in vitro. Sci Rep 1:242Google Scholar
  24. Devi JS, Bhimba BV, Ratnam K (2012) In vitro anticancer activity of silver nanoparticles synthesized using the extract of Gelidiella sp. Int J Pharm Pharm Sci 4:710–715Google Scholar
  25. Dobson PD, Kell DB (2008) Carrier-mediated cellular uptake of pharmaceutical drugs: an exception or the rule? Nat Rev Drug Discov 7:205Google Scholar
  26. El-Kassas HY, El-Sheekh MM (2014) Cytotoxic activity of biosynthesized gold nanoparticles with an extract of the red seaweed Corallina officinalis on the MCF-7 human breast cancer cell line. Asian Pac J Cancer Prev 15:4311–4317CrossRefGoogle Scholar
  27. Fabrowska J, Messyasz B, Szyling J, Walkowiak J, Łęska B (2018) Isolation of chlorophylls and carotenoids from freshwater algae using different extraction methods. Phycol Res 66:52–57CrossRefGoogle Scholar
  28. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386CrossRefGoogle Scholar
  29. Fernández Freire P, Peropadre A, Martín JMP, Herrero O, Hazen MJ (2009) An integrated cellular model to evaluate cytotoxic effects in mammalian cell lines. Toxicol in Vitro 23:1553–1558CrossRefGoogle Scholar
  30. Gajendran B, Chinnasamy A, Durai P, Raman J, Ramar M (2014) Biosynthesis and characterization of silver nanoparticles from Datura inoxia and its apoptotic effect on human breast cancer cell line MCF7. Mater Lett 122:98–102CrossRefGoogle Scholar
  31. Gul-e-Saba, Abdullah MA (2015) Polymeric nanoparticle mediated targeted drug delivery to cancer cells. In: Thangadurai D, Sangeetha J (eds) Biotechnology and Bioinformatics: Advances and Applications for Bioenergy, Bioremediation, and Biopharmaceutical Research. CRC Press / Apple Academic Press, New Jersey, USA, pp 301–344Google Scholar
  32. Gurunathan S, Han J, Eppakayala V, Jeyaraj M, Kim JH (2013) Cytotoxicity of biologically synthesized silver nanoparticles in MDA-MB-231 human breast cancer cells. Biomed Res Int 2013:10CrossRefGoogle Scholar
  33. Hajiaghaalipour F, Bagheri E, Faraj FL, Abdulla MA, Abdul Majid N (2017) Underlying mechanism for the modulation of apoptosis induced by a new benzoindole derivative on HT-29 colon cancer cells. RSC Adv 7:38257–38263CrossRefGoogle Scholar
  34. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770–776CrossRefGoogle Scholar
  35. Hussein HA, Abdullah MA (2019) Antioxidant activities of microalgal crude extracts (Personal communication)Google Scholar
  36. Hussein HA, Mohamad H, Ghazaly MM, Laith AA, Abdullah MA (2019) Cytotoxic effects of Nannochloropsis oculata and Chlorella sp. extracts with silver nanoparticles co-application on MCF-7 and 4T1 breast cancer cells without affecting normal Vero cells. (Personal communication)Google Scholar
  37. Hwang YJ, Lee EJ, Kim HR, Hwang KA (2013) Molecular mechanisms of luteolin-7-o-glucoside-induced growth inhibition on human liver cancer cells: G2/m cell cycle arrest and caspase-independent apoptotic signaling pathways. BMB Rep 46:611–616CrossRefGoogle Scholar
  38. Jayappriyan KR, Rajkumar R, Venkatakrishnan V, Nagaraj S, Rengasamy R (2013) In vitro anticancer activity of natural β-carotene from Dunaliella salina EU5891199 in PC-3 cells. Biomed Prev Nutr 3:99–105CrossRefGoogle Scholar
  39. Jung K, Won Y, Park S, Kong H, Sung J, Shin H, Park E, Lee JS (2009) Cancer statistics in Korea: Incidence, mortality and survival in 2005. J Korean Med Sci 24:995–1003CrossRefGoogle Scholar
  40. Kajani AA, Bordbar A, Hamid S, Esfahani Z, Khosropour AR, Razmjou A (2014) Green synthesis of anisotropic silver nanoparticles with potent anticancer activity using Taxus baccata extract. RSC Adv 4:61394–61403CrossRefGoogle Scholar
  41. Kaler A, Jain S, Banerjee UC (2013) Green and rapid synthesis of anticancerous silver nanoparticles by Saccharomyces boulardii and insight into mechanism of nanoparticle synthesis. Biomed Res Int 2013:8CrossRefGoogle Scholar
  42. Kannan RRR, Arumugam R, Anantharaman P (2010) Antibacterial potential of three seagrasses against human pathogens. Asian Pac J Trop Med 3:890–893CrossRefGoogle Scholar
  43. Kass GEN, Eriksson JE, Weis M, Orrenius S, Chow SC (1996) Chromatin condensation during apoptosis requires ATP. Biochem J 318:749–752CrossRefGoogle Scholar
  44. Kawasaki ES, Player TA (2005) Nanotechnology, nanomedicine, and the development of new, effective therapies for cancer. Nanomedicine 1:101–109CrossRefGoogle Scholar
  45. Kim YS, Li XF, Kang KH, Ryu B, Kim SK (2014) Stigmasterol isolated from marine microalgae Navicula incerta induces apoptosis in human hepatoma HepG2 cells. BMB Rep 47:433–438CrossRefGoogle Scholar
  46. Kumarihamy M, Ferreira D, Jr EMC, Sahu R, Tekwani BL, Duke SO, Khan S, Techen N, Nanayakkara NPD (2019) Antiplasmodial and cytotoxic cytochalasins from an endophytic fungus, Nemania sp. UM10M, isolated from a diseased Torreya taxifolia leaf. Molecules 24:777CrossRefGoogle Scholar
  47. Kravtsov BVD, Greer JP, Whitlock JA, Koury MJ (1998) Use of the microculture kinetic assay of apoptosis to determine chemosensitivities of leukemias. Blood 92:968–980Google Scholar
  48. Kurbacher CM, Cree IA, Bruckner HW, Brenne U, Kurbacher JA, Müller K, Mallmann PK (1998) Use of an ex vivo ATP luminescence assay to direct chemotherapy for recurrent ovarian cancer. Anti-Cancer Drugs 9:51–57CrossRefGoogle Scholar
  49. Kwon MJ, Nam TJ (2007) A polysaccharide of the marine alga Capsosiphon fulvescens induces apoptosis in AGS gastric cancer cells via an IGF-IR-mediated PI3K/Akt pathway. Cell Biol Int 31:768775 CrossRefGoogle Scholar
  50. Lammers T, Kiessling F, Hennink WE, Storm G (2012) Drug targeting to tumors: principles, pitfalls and (pre-) clinical progress. J Control Release 161:175–187CrossRefGoogle Scholar
  51. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185:1481–1486CrossRefGoogle Scholar
  52. Lezcano V, Fernández C, Parodi ER, Morelli S (2018) Antitumor and antioxidant activity of the freshwater macroalga Cladophora surera. J Appl Phycol 30:2913–2921CrossRefGoogle Scholar
  53. Magdi HM, Mourad MHE, Abd El-Aziz MM (2014) Biosynthesis of silver nanoparticles using fungi and biological evaluation of mycosynthesized silver nanoparticles. Egypt J Exp Biol 10:1–12Google Scholar
  54. Martínez Andrade K, Lauritano C, Romano G, Ianora A (2018) Marine microalgae with anti-cancer properties. Mar Drugs 16:165CrossRefGoogle Scholar
  55. Mashjoor S, Yousefzadi M, Esmaeili MA, Rafie R (2015) Cytotoxicity and antimicrobial activity of marine macro algae (Dictyotaceae and Ulvaceae) from the Persian Gulf. Cytotechnology 68:1717–1726CrossRefGoogle Scholar
  56. Mayer AMS, Gustafson KR (2008) Marine pharmacology in 2001–2: antitumour and cytotoxic compounds. Eur J Cancer 44:2357–2387CrossRefGoogle Scholar
  57. Mimeault M, Jouy N, Depreux P, Hénichart JP (2005) Synergistic antiproliferative and apoptotic effects induced by mixed epidermal growth factor receptor inhibitor ZD1839 and nitric oxide donor in human prostatic cancer cell lines. Prostate 62:187–199CrossRefGoogle Scholar
  58. Minchinton AI, Tannock IF (2006) Drug penetration in solid tumours. Nat Rev Cancer 6:583–592CrossRefGoogle Scholar
  59. Mohanta YK, Panda SK, Jayabalan R, Sharma N, Bastia AK, Mohanta TK (2017) Antimicrobial, antioxidant and cytotoxic activity of silver nanoparticles synthesized by leaf extract of Erythrina suberosa (Roxb.). Front Mol Biosci 4:14CrossRefGoogle Scholar
  60. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63CrossRefGoogle Scholar
  61. Moussavou G, Kwak DH, Obiang-Obonou BW, Maranguy CAO, Dinzouna-Boutamba SD, Lee DH, Pissibanganga OGM, Ko K, Seo JI, Choo YK (2014) Anticancer effects of different seaweeds on human colon and breast cancers. Mar Drugs 12:4898–4911CrossRefGoogle Scholar
  62. Namvar F, Mohamad R, Baharara J, Zafar-balanejad S, Fargahi F, Rahman HS (2013) Antioxidant, antiproliferative, and antiangiogenesis effects of polyphenol-rich seaweed (Sargassum muticum). Biomed Res Int 2013:9CrossRefGoogle Scholar
  63. Nigjeh SE, Yusoff F, Alitheen NBM, Rasoli M, Keong YS, Omar ARB (2013) Cytotoxic effect of ethanol extract of microalga, Chaetoceros calcitrans, and its mechanisms in inducing apoptosis in human breast cancer cell line. Biomed Res Int 2013:8Google Scholar
  64. Otunola GA, Afolayan AJ (2018) In vitro antibacterial, antioxidant and toxicity profile of silver nanoparticles green-synthesized and characterized from aqueous extract of a spice blend formulation. Biotechnol Biotechnol Equip 32:724–733CrossRefGoogle Scholar
  65. Preethy CP, Padmapriya R, Periasamy VS, Srinag S, Krishnamurthy H, Alshatwi AA, Akbarsha A (2012) Antiproliferative property of n-hexane and chloroform extracts of Anisomeles malabarica (L). R. Br. in HPV16-positive human cervical cancer cells. J Pharmacol Pharmacother 3:26–35CrossRefGoogle Scholar
  66. Rajendran N, Karpanai Selvan B, Sobana Piriya P, Logeswari V, Kathiresan E, Tamilselvi A, John Vennison S (2014) Phytochemicals, antimicrobial and antioxidant screening from five different marine microalgae. J Chem Pharm Sci:78–85Google Scholar
  67. Rashidipour M, Heydari R (2015) Biosynthesis of silver nanoparticles using extract of olive leaf: synthesis and in vitro cytotoxic effect on MCF-7 cells. J Nanostruct Chem 4:112CrossRefGoogle Scholar
  68. Rezakhani L, Rashidi Z, Mirzapur P, Khazaei M (2014) Antiproliferatory effects of crab shell extract on breast cancer cell line (MCF7). J Breast Cancer 17:219–225CrossRefGoogle Scholar
  69. Rosarin FS, Arulmozhi V, Nagarajan S, Mirunalini S (2013) Antiproliferative effect of silver nanoparticles synthesized using amla on Hep2 cell line. Asian Pac J Trop Med 6:1–10CrossRefGoogle Scholar
  70. Rouhimoghadam M, Safarian S, Carroll JS, Sheibani N, Bidkhori G (2018) Tamoxifen-induced apoptosis of MCF-7 Cells via GPR30/PI3K/MAPKs interactions: verification by ODE modeling and RNA sequencing. Front Physiol 9:907CrossRefGoogle Scholar
  71. Sansone C, Galasso C, Orefice I, Nuzzo G, Luongo E, Cutignano A, Romano G, Brunet C, Fontana A, Esposito F, Ianora A (2017) The green microalga Tetraselmis suecica reduces oxidative stress and induces repairing mechanisms in human cells. Sci Rep 7:41215CrossRefGoogle Scholar
  72. Schlinkert P, Casals E, Boyles M, Tischler U, Hornig E, Tran N, Zhao J, Himly M, Riediker M, Oostingh GJ, Puntes V, Duschl A (2015) The oxidative potential of differently charged silver and gold nanoparticles on three human lung epithelial cell types. J Nanobiotechnol 13:1–18CrossRefGoogle Scholar
  73. Selvi BCG, Madhavan J, Santhanam A (2016) Cytotoxic effect of silver nanoparticles synthesized from Padina tetrastromatica on breast cancer cell line. Adv Nat Sci Nanosci Nanotechnol 7:035015CrossRefGoogle Scholar
  74. Selvi KV, Sivakumar T (2014) Antihelminthic, anticancer, antioxidant activity of silver nanoparticles isolated from F. oxysporum. Int J Curr Res Chem Pharm Sci 1:105–111Google Scholar
  75. Shavandi Z, Ghazanfari T, Moghaddam KN (2011) In vitro toxicity of silver nanoparticles on murine peritoneal macrophages. Immunopharmacol Immunotoxicol 33:135–140CrossRefGoogle Scholar
  76. Shawkey AM, Rabeh MA, Abdulall AK, Abdellatif AO (2013) Green nanotechnology: anticancer activity of silver nanoparticles using Citrullus colocynthis aqueous extracts. Adv Life Sci Technol 13:60–71Google Scholar
  77. Siddiqui S, Ahmad R, Khan MA, Upadhyay S, Husain I, Srivastava AN (2019) Cytostatic and anti-tumor potential of ajwa date pulp against human hepatocellular carcinoma HepG2 cells. Sci Rep 9:245CrossRefGoogle Scholar
  78. Sit NW, Chan YS, Lai SC, Lim LN, Looi GT, Tay PL, Tee YT, Woon YY, Khoo KS, Ong HC (2018) In vitro antidermatophytic activity and cytotoxicity of extracts derived from medicinal plants and marine algae. J Mycol Med 28:561–567CrossRefGoogle Scholar
  79. Sivasubramanian R, Brindha P (2013) In-vitro cytotoxic, antioxidant and GC-MS studies on Centratherum punctatum Cass. Int J Pharm Pharm Sci 5:364–367Google Scholar
  80. Sombatsri A, Thummanant Y, Sribuhom T, Wongphakham P, Senawong T, Yenjai C (2019) Atalantums H-K from the peels of Atalantia monophylla and their cytotoxicity. Nat Prod Res:1–7Google Scholar
  81. Stanojković TP, Šavikin K, Zdunić G, Kljajić Z, Anti J (2013) In vitro antitumoral activities of Padina pavonia on human cervix and breast cancer cell lines. J Med Plant Res 7:419–424Google Scholar
  82. Sunita A, Manju S (2017) Phytochemical examination and GC-MS analysis of methanol and ethyl-acetate extract of root and stem of Gisekia Pharnaceoides Linn. Res J Pharm, Biol Chem Sci 8:168–174Google Scholar
  83. Supraja N, Prasad TNVKV, Soundariya M, Babujanarthanam R (2016) Synthesis, characterization and dose dependent antimicrobial and anti-cancerous activity of phycogenic silver nanoparticles against human hepatic carcinoma (HepG2) cell line. AIMS Bioeng 3:425–440CrossRefGoogle Scholar
  84. Suresh AK, Pelletier DA, Wang W, Morrell-Falvey JL, Gu B, Doktycz MJ (2012) Cytotoxicity induced by engineered silver nanocrystallites is dependent on surface coatings and cell types. Langmuir 28:2727–2735CrossRefGoogle Scholar
  85. Swamy MK, Sinniah UR (2015) A comprehensive review on the phytochemical constituents and pharmacological activities of Pogostemon cablin Benth.: an aromatic medicinal plant of industrial importance. Molecules 20:8521–8547CrossRefGoogle Scholar
  86. Szliszka E, Czuba ZP, Jernas K, Król W (2008) Dietary flavonoids sensitize HeLa cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). Int J Mol Sci 9:56–64CrossRefGoogle Scholar
  87. Tabata Y, Ikada Y (1988) Macrophage phagocytosis of biodegradable microspheres composed of L-lactic acidlglycolic acid homo- and copolymers. J Biomed Mater Res 22:837–858CrossRefGoogle Scholar
  88. Tait L, Soule HD, Russo J (1990) Ultrastructural and immunocytochemical characterization of an immortalized human breast epithelial cell line, MCF-10. Cancer Res 50:6087–6095Google Scholar
  89. Tiyaboonchai W (2003) Chitosan nanoparticles: a promising system for drug delivery. Naresuan Univ J 11:51–66Google Scholar
  90. Tsujimoto Y (1997) Apoptosis and necrosis: intracellular ATP level as a determinant for cell death modes. Cell Death Differ 4:429–434CrossRefGoogle Scholar
  91. Venkara Raman B, Samuel LA, Pardha Saradhi M, Narashimha Rao B, Naga Vamsi Krishna A, Sudhakar M, Radhakrishnan TM (2012) Antibacterial, antioxidant activity and GC-MS analysis of Eupatorium odoratum. Asian J Pharm Clin Res 5:99–106Google Scholar
  92. Vivek R, Thangam R, Muthuchelian K, Gunasekaran P, Kaveri K, Kannan S (2012) Green biosynthesis of silver nanoparticles from Annona squamosa leaf extract and its in vitro cytotoxic effect on MCF-7 cells. Process Biochem 47:2405–2410CrossRefGoogle Scholar
  93. Wei LS, Wee W, Siong JYF, Syamsumir DF (2011) Characterization of anticancer, antimicrobial, antioxidant properties and chemical compositions of Peperomia pellucida leaf extract. Acta Med Iran 49:670–674Google Scholar
  94. Wicki A, Witzigmann D, Balasubramanian V, Huwyler J (2015) Nanomedicine in cancer therapy: challenges, opportunities, and clinical applications. J Control Release 200:138–157CrossRefGoogle Scholar
  95. Williams HD, Trevaskis NL, Charman SA, Shanker RM, Charman WN, Pouton CW, Porter CJH (2013) Strategies to address low drug solubility in discovery and development. Pharmacol Rev 65:315–499CrossRefGoogle Scholar
  96. Yasuhara N, Eguchi Y, Tachibana T, Imamoto N, Yoneda Y, Tsujimoto Y (1997) Essential role of active nuclear transport in apoptosis. Genes Cells 2:55–64CrossRefGoogle Scholar
  97. Yu FR, Lian XZ, Guo HY, McGuire PM, Li RD, Wang R, Yu FH (2005) Isolation and characterization of methyl esters and derivatives from Euphorbia kansui (Euphorbiaceae) and their inhibitory effects on the human SGC-7901 cells. Pharm Pharm Sci 8:528–535Google Scholar
  98. Yusof YAM, Saad SM, Makpol S, Shamaan NA, Ngah WZW (2010) Hot water extract of Chlorella vulgaris induced DNA damage and apoptosis. Clinics 65:1371–1377CrossRefGoogle Scholar
  99. Zhang XQ, Xu X, Bertrand N, Pridgen E, Swami A, Farokhzad OC (2012) Interactions of nanomaterials and biological systems : implications to personalized nanomedicine. Adv Drug Deliv Rev 64:1363–1384CrossRefGoogle Scholar
  100. Zhou C, Shen Q, Xue J, Ji C, Chen J (2013) Overexpression of TTRAP inhibits cell growth and induces apoptosis in osteosarcoma cells. BMB Rep 46:113–118CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Institute of Marine BiotechnologyUniversiti Malaysia TerengganuKuala NerusMalaysia
  2. 2.College of DentistryUniversity of BasrahBasrahIraq
  3. 3.School of Fundamental ScienceUniversiti Malaysia TerengganuKuala NerusMalaysia
  4. 4.School of Fisheries and Aquaculture SciencesUniversiti Malaysia TerengganuKuala NerusMalaysia

Personalised recommendations