Synthesis and Characterization of a Walnut Peptides-Zinc Complex and Its Antiproliferative Activity against Human Breast Carcinoma Cells through the Induction of Apoptosis

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 7, 2016, Pages 1509-1519

  Liao, Wenzhen ^a   Lai, Ting ^a   Chen, Luying ^a   Fu, Junning ^b   Sreenivasan, Sreeprasad T ^c   Yu, Zhiqiang ^d   Ren, Jiaoyan ^a  

^a SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

^b JINAN UNIVERSITY   (China)

^c Rice University   (United States)

^d SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

antitumor; apoptosis; biosynthesis; walnut peptides zinc complex

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; CELL CULTURE; CELL DEATH; CELL MEMBRANES; CELL PROLIFERATION; CELLS; CYTOLOGY; PEPTIDES;

ANTI-PROLIFERATIVE; ANTI-PROLIFERATIVE ACTIVITIES; ANTI-TUMORS; BIOACTIVE PEPTIDES; CELL SURFACE RECEPTORS; HUMAN BREAST CARCINOMA CELLS; SYNTHESIS AND CHARACTERIZATIONS; ZINC COMPLEX;

ZINC;

GROWTH INHIBITOR; PEPTIDE; ZINC;

APOPTOSIS; BREAST NEOPLASMS; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; FEMALE; HUMAN; PATHOPHYSIOLOGY; SYNTHESIS; TUMOR CELL LINE; WALNUT;

APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; GROWTH INHIBITORS; HUMANS; JUGLANS; PEPTIDES; ZINC;

EID: 84959084423     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b04924     Document Type: Article

References (56)

1. Wang, L. S.; Huang, J. C.; Chen, Y. L.; Huang, M.; Zhou, G. H. Identification and Characterization of Antioxidant Peptides from Enzymatic Hydrolysates of Duck Meat J. Agric. Food Chem. 2015, 63, 3437-3444 10.1021/jf506120w
2. Ambigaipalan, P.; Shahidi, F. Antioxidant Potential of Date (Phoenix dactylifera L.) Seed Protein Hydrolysates and Carnosine in Food and Biological Systems J. Agric. Food Chem. 2015, 63, 864-871 10.1021/jf505327b
3. Meisel, H. Multifunctional peptides encrypted in milk proteins BioFactors 2004, 21, 55-61 10.1002/biof.552210111
4. Wen, Y.; Meng, W. Recent In Vivo Evidences of Particle-Based Delivery of Small-Interfering RNA (siRNA) into Solid Tumors J. Pharm. Innov. 2014, 9, 158-173 10.1007/s12247-014-9183-4
5. García-Tejedor, A.; Sánchez-Rivera, L.; Castelló-Ruiz, M.; Recio, I.; Salom, J. B.; Manzanares, P. Novel antihypertensive lactoferrin-derived peptides produced by Kluyveromyces marxianus: gastrointestinal stability profile and in vivo angiotensin I-converting enzyme (ACE) inhibition J. Agric. Food Chem. 2014, 62, 1609-1616 10.1021/jf4053868
6. Wen, Y.; Kolonich, H. R.; Kruszewski, K. M.; Giannoukakis, N.; Gawalt, E. S.; Meng, W. S. Retaining Antibodies in Tumors with a Self-Assembling Injectable System Mol. Pharmaceutics 2013, 10, 1035-1044 10.1021/mp300504z
7. McGranahan, G.; Leslie, C. Walnut. In Fruit Breeding; Springer: New York, 2012; pp 827-846.
8. Carvalho, M.; Ferreira, P. J.; Mendes, V. S.; Silva, R.; Pereira, J. A.; Jerónimo, C.; Silva, B. M. Human cancer cell antiproliferative and antioxidant activities of Juglans regia L Food Chem. Toxicol. 2010, 48, 441-447 10.1016/j.fct.2009.10.043
9. Mukuddem-Petersen, J.; Stonehouse (Oosthuizen), W.; Jerling, J. C.; Hanekom, S. M.; White, Z. Effects of a high walnut and high cashew nut diet on selected markers of the metabolic syndrome: a controlled feeding trial Br. J. Nutr. 2007, 97, 1144-1153 10.1017/S0007114507682944
10. Salcedo, C. L.; Lopez de Mishima, B. A.; Nazareno, M. A. Walnuts and almonds as model systems of foods constituted by oxidisable, pro-oxidant and antioxidant factors Food Res. Int. 2010, 43, 1187-1197 10.1016/j.foodres.2010.02.016
11. Kiran Aithal, A. B.; Sunil Kumar, M. R.; Nageshwar Rao, B.; Udupa, N.; Satish Rao, B. S. Juglone, a naphthoquinone from walnut, exerts cytotoxic and genotoxic effects against cultured melanoma tumor cells Cell Biol. Int. 2009, 33, 1039-1049 10.1016/j.cellbi.2009.06.018
12. Joseph, J. A.; Shukitt-Hale, B.; Willis, L. M. Grape juice, berries, and walnuts affect brain aging and behavior J. Nutr. 2009, 139, 1813S-1817S 10.3945/jn.109.108266
13. Jamdar, S.; Rajalakshmi, V.; Pednekar, M.; Juan, F.; Yardi, V.; Sharma, A. Influence of degree of hydrolysis on functional properties, antioxidant activity and ACE inhibitory activity of peanut protein hydrolysate Food Chem. 2010, 121, 178-184 10.1016/j.foodchem.2009.12.027
14. Chen, N.; Yang, H.; Sun, Y.; Niu, J.; Liu, S. Purification and identification of antioxidant peptides from walnut (Juglans regia L.) protein hydrolysates Peptides 2012, 38, 344-349 10.1016/j.peptides.2012.09.017
15. Liu, M.; Du, M.; Zhang, Y.; Xu, W.; Wang, C.; Wang, K.; Zhang, L. Purification and identification of an ACE inhibitory peptide from walnut protein J. Agric. Food Chem. 2013, 61, 4097-4100 10.1021/jf4001378
16. Ken, C.-F.; Cheng, Y.-F.; Chang, C.-F.; Lin, C.-T. Copper/zinc-superoxide dismutase from Epinephelus malabaricus cDNA and enzyme property J. Agric. Food Chem. 2003, 51, 5688-5694 10.1021/jf030162p
17. Sreenivasulu, K.; Raghu, P.; Ravinder, P.; Nair, K. M. Effect of Dietary Ligands and Food Matrices on Zinc Uptake in Caco-2 Cells: Implications in Assessing Zinc Bioavailability J. Agric. Food Chem. 2008, 56, 10967-10972 10.1021/jf802060q
18. Wysokinski, D.; Blasiak, J.; Wozniak, K. Zinc differentially modulates DNA damage induced by anthracyclines in normal and cancer cells Exp. Oncol. 2012, 34, 327-331
19. Haase, H.; Mazzatti, D. J.; White, A.; Ibs, K. H.; Engelhardt, G.; Hebel, S.; Powell, J. R.; Rink, L. Differential gene expression after zinc supplementation and deprivation in human leukocyte subsets Mol. Med. 2007, 13, 362
20. Prasad, A. S. Zinc in human health: an update J. Trace Elem. Exp. Med. 1998, 11, 63-87 10.1002/(SICI)1520-670X(1998)11:2/3<63::AID-JTRA2>3.0.CO;2-5
21. Fischer Walker, C.; Ezzati, M.; Black, R. Global and regional child mortality and burden of disease attributable to zinc deficiency Eur. J. Clin. Nutr. 2009, 63, 591-597 10.1038/ejcn.2008.9
22. Hambidge, K. M.; Krebs, N. F. Zinc deficiency: a special challenge J. Nutr. 2007, 137, 1101-1105
23. Alam, S.; Kelleher, S. L. Cellular mechanisms of zinc dysregulation: a perspective on zinc homeostasis as an etiological factor in the development and progression of breast cancer Nutrients 2012, 4, 875-903 10.3390/nu4080875
24. Li, M.; Zhang, Y.; Liu, Z.; Bharadwaj, U.; Wang, H.; Wang, X.; Zhang, S.; Liuzzi, J. P.; Chang, S.-M.; Cousins, R. J. Aberrant expression of zinc transporter ZIP4 (SLC39A4) significantly contributes to human pancreatic cancer pathogenesis and progression Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 18636-18641 10.1073/pnas.0709307104
25. Mihelich, B. L.; Khramtsova, E. A.; Arva, N.; Vaishnav, A.; Johnson, D. N.; Giangreco, A. A.; Martens-Uzunova, E.; Bagasra, O.; Kajdacsy-Balla, A.; Nonn, L. miR-183-96-182 cluster is overexpressed in prostate tissue and regulates zinc homeostasis in prostate cells J. Biol. Chem. 2011, 286, 44503-44511 10.1074/jbc.M111.262915
26. Nardinocchi, L.; Pantisano, V.; Puca, R.; Porru, M.; Aiello, A.; Grasselli, A.; Leonetti, C.; Safran, M.; Rechavi, G.; Givol, D. Zinc downregulates HIF-1α and inhibits its activity in tumor cells in vitro and in vivo PLoS One 2010, 5, e15048 10.1371/journal.pone.0015048
27. Chuang, S.-M.; Wang, H.-F.; Hsiao, C.-C.; Cherng, S.-H. Zinc ion enhances GABA tea-mediated oxidative DNA damage J. Agric. Food Chem. 2012, 60, 1586-1594 10.1021/jf2044263
28. Franklin, R. B.; Costello, L. C. Zinc as an anti-tumor agent in prostate cancer and in other cancers Arch. Biochem. Biophys. 2007, 463, 211-217 10.1016/j.abb.2007.02.033
29. Feng, P.; Li, T.; Guan, Z.; Franklin, R. B.; Costello, L. C. The involvement of Bax in zinc-induced mitochondrial apoptogenesis in malignant prostate cells Mol. Cancer 2008, 7, 25 10.1186/1476-4598-7-25
30. Franklin, R. B.; Costello, L. C. The important role of the apoptotic effects of zinc in the development of cancers J. Cell. Biochem. 2009, 106, 750-757 10.1002/jcb.22049
31. Costello, L.; Franklin, R.; Feng, P. Mitochondrial function, zinc, and intermediary metabolism relationships in normal prostate and prostate cancer Mitochondrion 2005, 5, 143-153 10.1016/j.mito.2005.02.001
32. Maret, W.; Sandstead, H. H. Zinc requirements and the risks and benefits of zinc supplementation J. Trace Elem. Med. Biol. 2006, 20, 3-18 10.1016/j.jtemb.2006.01.006
33. Plum, L. M.; Rink, L.; Haase, H. The essential toxin: impact of zinc on human health Int. J. Environ. Res. Public Health 2010, 7, 1342-1365 10.3390/ijerph7041342
34. Anbu, S.; Kamalraj, S.; Varghese, B.; Muthumary, J.; Kandaswamy, M. A series of oxyimine-based macrocyclic dinuclear zinc (II) complexes enhances phosphate ester hydrolysis, DNA binding, DNA hydrolysis, and lactate dehydrogenase inhibition and induces apoptosis Inorg. Chem. 2012, 51, 5580-5592 10.1021/ic202451e
35. Bolfarini, G. C.; Siqueira-Moura, M. P.; Demets, G. J.; Morais, P. C.; Tedesco, A. C. In vitro evaluation of combined hyperthermia and photodynamic effects using magnetoliposomes loaded with cucurbituril zinc phthalocyanine complex on melanoma J. Photochem. Photobiol., B 2012, 115, 1-4 10.1016/j.jphotobiol.2012.05.009
36. Nagy, E. M.; Sitran, S.; Montopoli, M.; Favaro, M.; Marchiò L.; Caparrotta, L.; Fregona, D. Zinc (II) complexes with dithiocarbamato derivatives: Structural characterisation and biological assays on cancerous cell lines J. Inorg. Biochem. 2012, 117, 131-139 10.1016/j.jinorgbio.2012.09.004
37. Sweigert, P.; Xu, Z.; Hong, Y.; Swavey, S. Nickel, copper, and zinc centered ruthenium-substituted porphyrins: effect of transition metals on photoinduced DNA cleavage and photoinduced melanoma cell toxicity Dalton T. 2012, 41, 5201-5208 10.1039/c2dt12331b
38. Terenzi, A.; Fanelli, M.; Ambrosi, G.; Amatori, S.; Fusi, V.; Giorgi, L.; Liveri, V. T.; Barone, G. DNA binding and antiproliferative activity toward human carcinoma cells of copper (II) and zinc (II) complexes of a 2, 5-diphenyl [1, 3, 4] oxadiazole derivative Dalton T. 2012, 41, 4389-4395 10.1039/c2dt11759b
39. Liao, W.; Lu, Y.; Fu, J.; Ning, Z.; Yang, J.; Ren, J. Preparation and Characterization of Dictyophora indusiata Polysaccharide-Zinc Complex and Its Augmented Antiproliferative Activity on Human Cancer Cells J. Agric. Food Chem. 2015, 63, 6525-6534 10.1021/acs.jafc.5b00614
40. Garufi, A.; Trisciuoglio, D.; Porru, M.; Leonetti, C.; Stoppacciaro, A.; D'Orazi, V.; Avantaggiati, M.; Crispini, A.; Pucci, D.; D'Orazi, G. A fluorescent curcumin-based Zn (II)-complex reactivates mutant (R175H and R273H) p53 in cancer cells J. Exp. Clin. Cancer Res. 2013, 32, 72 10.1186/1756-9966-32-72
41. Milacic, V.; Chen, D.; Giovagnini, L.; Diez, A.; Fregona, D.; Dou, Q. P. Pyrrolidine dithiocarbamate-zinc (II) and-copper (II) complexes induce apoptosis in tumor cells by inhibiting the proteasomal activity Toxicol. Appl. Pharmacol. 2008, 231, 24-33 10.1016/j.taap.2008.03.009
42. Wang, H.; Joseph, J. A. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader Free Radical Biol. Med. 1999, 27, 612-616 10.1016/S0891-5849(99)00107-0
43. Shi, Y. A structural view of mitochondria-mediated apoptosis Nat. Struct. Biol. 2001, 8, 394-401 10.1038/87548
44. Cvek, B.; Milacic, V.; Taraba, J.; Dou, Q. P. Ni (II), Cu (II), and Zn (II) diethyldithiocarbamate complexes show various activities against the proteasome in breast cancer cells J. Med. Chem. 2008, 51, 6256-6258 10.1021/jm8007807
45. Clarke, P. G. Apoptosis versus Necrosis. In Cell Death and Diseases of the Nervous System; Springer: New York, 1999; pp 3-28.
46. Golstein, P.; Kroemer, G. Cell death by necrosis: towards a molecular definition Trends Biochem. Sci. 2007, 32, 37-43 10.1016/j.tibs.2006.11.001
47. Schutte, B.; Nuydens, R.; Geerts, H.; Ramaekers, F. Annexin V binding assay as a tool to measure apoptosis in differentiated neuronal cells J. Neurosci. Methods 1998, 86, 63-69 10.1016/S0165-0270(98)00147-2
48. Kalejta, R. F.; Shenk, T.; Beavis, A. J. Use of a membrane-localized green fluorescent protein allows simultaneous identification of transfected cells and cell cycle analysis by flow cytometry Cytometry 1997, 29, 286-291 10.1002/(SICI)1097-0320(19971201)29:4<286::AID-CYTO4>3.0.CO;2-8
49. Xu, X.; Hamhouyia, F.; Thomas, S. D.; Burke, T. J.; Girvan, A. C.; McGregor, W. G.; Trent, J. O.; Miller, D. M.; Bates, P. J. Inhibition of DNA replication and induction of S phase cell cycle arrest by G-rich oligonucleotides J. Biol. Chem. 2001, 276, 43221-43230 10.1074/jbc.M104446200
50. Petronilli, V.; Penzo, D.; Scorrano, L.; Bernardi, P.; Di Lisa, F. The mitochondrial permeability transition, release of cytochrome c and cell death correlation with the duration of pore openings in situ J. Biol. Chem. 2001, 276, 12030-12034 10.1074/jbc.M010604200
51. Gerald, K. Cell and Molecular Biology: Concepts and Experiments; John Wiley and Sons: Hoboken, NJ, 2005.
52. Bishop, G. M.; Dringen, R.; Robinson, S. R. Zinc stimulates the production of toxic reactive oxygen species (ROS) and inhibits glutathione reductase in astrocytes Free Radical Biol. Med. 2007, 42, 1222-1230 10.1016/j.freeradbiomed.2007.01.022
53. Wiseman, D. A.; Wells, S. M.; Hubbard, M.; Welker, J. E.; Black, S. M. Alterations in zinc homeostasis underlie endothelial cell death induced by oxidative stress from acute exposure to hydrogen peroxide Am. J. Physiol. Lung Cell Mol. Physiol. 2007, 292, L165-L177 10.1152/ajplung.00459.2005
54. Wong, S. W.; Leung, P. T.; Djurišić, A.; Leung, K. M. Toxicities of nano zinc oxide to five marine organisms: influences of aggregate size and ion solubility Anal. Bioanal. Chem. 2010, 396, 609-618 10.1007/s00216-009-3249-z
55. Song, W.; Zhang, J.; Guo, J.; Zhang, J.; Ding, F.; Li, L.; Sun, Z. Role of the dissolved zinc ion and reactive oxygen species in cytotoxicity of ZnO nanoparticles Toxicol. Lett. 2010, 199, 389-397 10.1016/j.toxlet.2010.10.003
56. Shi, Y. Mechanisms of caspase activation and inhibition during apoptosis Mol. Cell 2002, 9, 459-470 10.1016/S1097-2765(02)00482-3