Divergent Anticancer Activity of Free and Formulated Camel Milk α-Lactalbumin

References

• Chen HY, Mollstedt O, Tsai MH, Kreider RB. Potential clinical applications of multi-functional milk proteins and peptides in cancer management. Curr Med Chem. 2014;21:2424–2437.
   PubMed Web of Science ®Google Scholar
• Svensson M, Duringer C, Hallgren O, Mossberg AK, Hakansson A, Linse S, et al. Hamlet–a complex from human milk that induces apoptosis in tumor cells but spares healthy cells. Adv Exp Med Biol. 2002;503:125–132.
   PubMed Web of Science ®Google Scholar
• Hakansson AP, Roche-Hakansson H, Mossberg AK, Svanborg C. Apoptosis-like death in bacteria induced by HAMLET, a human milk lipid-protein complex. PLoS One. 2011;6:e17717.
   PubMed Web of Science ®Google Scholar
• Yoo YC, Watanabe R, Koike Y, Mitobe M, Shimazaki K, Watanabe S, et al. Apoptosis in human leukemic cells induced by lactoferricin, a bovine milk protein-derived peptide: involvement of reactive oxygen species. Biochem Biophys Res Commun. 1997;237:624–628.
   PubMed Web of Science ®Google Scholar
• Hakansson A, Zhivotovsky B, Orrenius S, Sabharwal H, Svanborg C. Apoptosis induced by a human milk protein. Proc Natl Acad Sci U S A. 1995;92:8064–8068.
   PubMed Web of Science ®Google Scholar
• Casbarra A, Birolo L, Infusini G, Dal Piaz F, Svensson M, Pucci P, et al. Conformational analysis of HAMLET, the folding variant of human alpha-lactalbumin associated with apoptosis. Protein Sci. 2004;13:1322–1330.
   PubMed Web of Science ®Google Scholar
• Fischer W, Gustafsson L, Mossberg AK, Gronli J, Mork S, Bjerkvig R, et al. Human alpha-lactalbumin made lethal to tumor cells (HAMLET) kills human glioblastoma cells in brain xenografts by an apoptosis-like mechanism and prolongs survival. Cancer Res. 2004;64:2105–2112.
   PubMed Web of Science ®Google Scholar
• Mossberg AK, Hun Mok K, Morozova-Roche LA, Svanborg C Structure and function of human alpha-lactalbumin made lethal to tumor cells (HAMLET)-type complexes. FEBS J. 2010;277:4614–4625.
   PubMed Web of Science ®Google Scholar
• Mossberg AK, Puchades M, Halskau O, Baumann A, Lanekoff I, Chao Y, et al. HAMLET interacts with lipid membranes and perturbs their structure and integrity. PLoS One. 2010;5:e9384.
   PubMed Web of Science ®Google Scholar
• Mossberg AK, Hou Y, Svensson M, Holmqvist B, Svanborg C HAMLET treatment delays bladder cancer development. J Urol. 2010;183:1590–1597.[https://doi.org/10.1016/j.juro.2009.12.008] PMID:20172551
   PubMed Web of Science ®Google Scholar
• Gustafsson L, Leijonhufvud I, Aronsson A, Mossberg AK, Svanborg C Treatment of skin papillomas with topical alpha-lactalbumin-oleic acid. N Engl J Med. 2004;350:2663–2672.
   PubMed Web of Science ®Google Scholar
• Mossberg AK, Wullt B, Gustafsson L, Mansson W, Ljunggren E, Svanborg C Bladder cancers respond to intravesical instillation of HAMLET (human alphalactalbumin made lethal to tumor cells). Int J Cancer. 2007;121:1352–1359.
   PubMed Web of Science ®Google Scholar
• Puthia M, Storm P, Nadeem A, Hsiung S, Svanborg C Prevention and treatment of colon cancer by peroral administration of HAMLET (human alpha-lactalbumin made lethal to tumor cells). Gut 2014;63:131–142.
   PubMed Web of Science ®Google Scholar
• Pettersson J, Mossberg AK, Svanborg C alpha-Lactalbumin species variation, HAMLET formation, and tumor cell death. Biochem Biophys Res Commun. 2006;345:260–270.
   PubMed Web of Science ®Google Scholar
• Atri MS, Saboury AA, Moosavi-Movahedi AA, Goliaei B, Sefidbakht Y, Alijanvand HH, et al. Structure and stability analysis of cytotoxic complex of camel alpha-lactalbumin and unsaturated fatty acids produced at high temperature. J Biomol Struct Dyn. 2011;28:919–928.
   PubMed Web of Science ®Google Scholar
• Permyakov SE, Pershikova IV, Khokhlova TI, Uversky VN, Permyakov EA No need to be HAMLET or BAMLET to interact with histones: binding of monomeric alpha-lactalbumin to histones and basic poly-amino acids. Biochemistry2004;43:5575–5582.
   PubMed Web of Science ®Google Scholar
• Svensson M, Fast J, Mossberg AK, Duringer C, Gustafsson L, Hallgren O, et al. Alpha-lactalbumin unfolding is not sufficient to cause apoptosis, but is required for the conversion to HAMLET (human alpha-lactalbumin made lethal to tumor cells). Protein Sci. 2003;12:2794–2804.
   PubMed Web of Science ®Google Scholar
• Nakamura T, Aizawa T, Kariya R, Okada S, Demura M, Kawano K, et al. Molecular mechanisms of the cytotoxicity of human alphalactalbumin made lethal to tumor cells (HAMLET) and other protein-oleic acid complexes. J Biol Chem. 2013;288:14408–14416.
   PubMed Web of Science ®Google Scholar
• Tolin S, De Franceschi G, Spolaore B, Frare E, Canton M, Polverino de Laureto P, et al. The oleic acid complexes of proteolytic fragments of alpha-lactalbumin displayy apoptotic activity. FEBS J. 2010;277:163–173.
   PubMed Web of Science ®Google Scholar
• Min S, Meehan J, Sullivan LM, Harte NP, Xie Y, Davey GP, et al. Alternatively folded proteins with unexpected beneficial functions. Biochem Soc Trans. 2012;40:746–751.
   PubMed Web of Science ®Google Scholar
• Redington JM, Breydo L, Almehdar HA, Redwan EM, Uversky VN alpha-Lactalbumin: of camels and cows. Protein Pept Lett. 2016;23:1072–1080.
   PubMed Web of Science ®Google Scholar
• Almahdy O, El-Fakharany EM, El-Dabaa E, Ng TB, Redwan EM Examination of the activity of camel milk casein against hepatitis C virus (genotype-4a) and its apoptotic potential in hepatoma and hela cell lines. Hepat Mon. 2011;11:724–730.
   PubMed Web of Science ®Google Scholar
• Atri MS, Saboury AA, Moosavi-Movahedi AA, Kavousi K, Ariaeenejad S Effects of zinc binding on the structure and thermal stability of camel alpha-lactalbumin. J Therm Anal Calorim. 2015;120:481–488.
   Web of Science ®Google Scholar
• Fang B, Zhang M, Tian M, Jiang L, Guo HY, Ren FZ Bovine lactoferrin binds oleic acid to form an anti-tumor complex similar to HAMLET. Biochim Biophys Acta. 2014;1841:535–543.
   PubMed Web of Science ®Google Scholar
• Duncombe WG The colorimetric micro-determination of long-chain fatty acids. Biochem J. 1963;88:7–10.
   PubMed Web of Science ®Google Scholar
• Redwan E Simple, sensitive and quick protocol to detect less than 1 ng of bacterial lipopolysaccharide. Prep Biochem Biotechnol. 2012;42:171–182.
   PubMed Web of Science ®Google Scholar
• Vistica DT, Skehan P, Scudiero D, Monks A, Pittman A, Boyd MR Tetrazolium-based assays for cellular viability: a critical examination of selected parameters affecting formazan production. Cancer Res. 1991;51:2515–2520.
   PubMed Web of Science ®Google Scholar
• Mosmann T Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65:55–63.
   PubMed Web of Science ®Google Scholar
• Jass JR, Mukawa K, Goh HS, Love SB, Capellaro D Clinical importance of DNA content in rectal cancer measured by flow cytometry. J Clin Pathol. 1989;42:254–259.
   PubMed Web of Science ®Google Scholar
• Cao P, Cai X, Lu W, Zhou F, Huo J Growth inhibition and induction of apoptosis in SHG-44 Glioma cells by chinese medicine formula “Pingliu Keli”. Evid Based Complement Alternat Med. 2011;2011:Article ID 958243, 9 pages.
   Web of Science ®Google Scholar
• Shanmugaprakash M, Jayashree C, Vinothkumar V, Senthilkumar SNS, Siddiqui S, Rawat V, et al. Biochemical characterization and antitumor activity of three phase partitioned L-asparaginase from Capsicum annuum L. Sep Purif Technol. 2015;142:258–267.
   Web of Science ®Google Scholar
• Chakravarti B, Maurya R, Siddiqui JA, Kumar Bid H, Rajendran SM, Yadav PP, et al. In vitro anti-breast cancer activity of ethanolic extract of Wrightia tomentosa: role of pro-apoptotic effects of oleanolic acid and urosolic acid. J Ethnopharmacol. 2012;142:72–79.
   PubMed Web of Science ®Google Scholar
• Permyakov EA, Permyakov SE, Breydo L, Redwan EM, Almehdar HA, Uversky VN Disorder in milk proteins: alpha-lactalbumin. Part C. peculiarities of metal binding. Curr Protein Pept Sci. 2016;17:735–745.
   PubMed Web of Science ®Google Scholar
• Permyakov EA, Permyakov SE, Breydo L, Redwan EM, Almehdar HA, Uversky VN Disorder in milk proteins: alpha -lactalbumin. Part A. Structural properties and conformational behavior. Curr Protein Pept Sci. 2016;17:352–367.
   PubMed Web of Science ®Google Scholar
• Uversky VN, Permyakov SE, Breydo L, Redwan EM, Almehdar HA, Permyakov EA Disorder in milk proteins: alpha-lactalbumin. Part B. A multifunctional whey protein acting as an oligomeric molten globular “Oil Container” in the anti-tumorigenic drugs, liprotides. Curr Protein Pept Sci. 2016;17:612–628.
   PubMed Web of Science ®Google Scholar
• Wehbi Z, Perez MD, Dalgalarrondo M, Sanchez L, Calvo M, Chobert JM, et al. Study of ethanol-induced conformational changes of holo and apo alphalactalbumin by spectroscopy and limited proteolysis. Mol Nutr Food Res. 2006;50:34–43.
   PubMed Web of Science ®Google Scholar
• Barbana C, Sanchez L, Perez MD Bioactivity of alpha-lactalbumin related to its interaction with fatty acids: a review. Crit Rev Food Sci Nutr. 2011;51:783–794.
   PubMed Web of Science ®Google Scholar
• Brinkmann CR, Thiel S, Otzen DE Protein-fatty acid complexes: biochemistry, biophysics and function. FEBS J. 2013;280:1733–1749.
   PubMed Web of Science ®Google Scholar
• Rath EM, Duff AP, Hakansson AP, Vacher CS, Liu GJ, Knott RB, et al. Structure and potential cellular targets of HAMLET-like anti-cancer compounds made from milk components. J Pharm Pharm Sci. 2015;18:773–824.
   PubMed Web of Science ®Google Scholar
• Pedersen JN, Pedersen JS, Otzen DE The use of liprotides to stabilize and transport hydrophobic molecules. Biochemistry. 2015;54:4815–4823.
   PubMed Web of Science ®Google Scholar
• Frislev HS, Jessen CM, Oliveira CL, Pedersen JS, Otzen DE Liprotides made of alpha-lactalbumin and cis fatty acids form core-shell and multi-layer structures with a common membrane-targeting mechanism. Biochim Biophys Acta. 2016;1864:847–859.
   PubMed Web of Science ®Google Scholar
• El Miniawya HMF, Ahmed KA, Mansourc SA, Khattab MMS Camel milk inhibits murine hepatic carcinogenesis, initiated by diethylnitrosamine and promoted by phenobarbitone. Pharm Biol. 2017;55:1513–1520.
   PubMed Web of Science ®Google Scholar
• Korashy HM, Maayah ZH, Abd-Allah AR, El-Kadi AOS, Alhaider AA J Biomed Biotechnol. 2012;2012:1–9.
   PubMedGoogle Scholar
• Habib HM, Ibrahim WH, Schneider-Stock R, Hassan HM Camel milk lactoferrin reduces the proliferation of colorectal cancer cells and exerts antioxidant and DNA damage inhibitory activities. Food Chem. 2013;141(1):148–152.
   PubMed Web of Science ®Google Scholar
• Tolin S, De Franceschi G, Spolaore B, Frare E, Canton M, de Polverino LP, et al. The oleic acid complexes of proteolytic fragments of alpha-lactalbumin display apoptotic activity. FEBS J. 2010;277: 163–173.
   PubMed Web of Science ®Google Scholar
• Hoque M, Dave S, Gupta P, Saleemuddin M Oleic acid may be the key contributor in the BAMLET-induced erythrocyte hemolysis and tumoricidal action. PLoS One. 2013;8:e68390–e68405.
   PubMed Web of Science ®Google Scholar
• Fang B, Zhang M, Wu H, Fan X, Ren F Internalization properties of the anti-tumor α-lactalbumin-oleic acid complex. Int J Biol Macromol. 2017;96:44–51.
   PubMed Web of Science ®Google Scholar
• Nakamura T, Aizawa T, Kariya R, Okada S, Demura M, Kawano K, et al. Molecular mechanisms of the cytotoxicity of human α-lactalbumin made lethal to tumor cells (HAMLET) and other protein-oleic acid complexes. J Biol Chem 2013;288(20):14408–14416.
   PubMed Web of Science ®Google Scholar
• Uversky VN, Permyakov SE, Breydo L, Redwan EM, Almehdar HA, Permyakov EA Disorder in milk proteins: α-lactalbumin. part b. a multifunctional whey protein acting as an oligomeric molten globular “oil container” in the anti-tumorigenic drugs, liprotides. Curr Protein Pept Sci. 2016;17(6):612–628.
   PubMed Web of Science ®Google Scholar
• Svanborg C, Agerstam H, Aronson A, Bjerkvig R, Duringer C, Fischer W, et al. HAMLET kills tumor cells by apoptosis-like mechanism-cellular, molecular, and therapeutic aspects. Adv Cancer Res. 2003;88:1–29.
   PubMed Web of Science ®Google Scholar
• Paul MK, Anup K, Mukhopadhyay AK Tyrosine kinase—role and significance in cancer. Int J Med Sci. 2004;1(2):101–115.
   PubMedGoogle Scholar
• Vlahovic G, Crawfor J Activation of tyrosine kinases in cancer. Oncologist. 2003;8:531–538.
   PubMed Web of Science ®Google Scholar
• El-Miligy MM, Abd El Razik HA, Abu-Serie MM. Synthesis of piperazine-based thiazolidinones as VEGFR2 tyrosine kinase inhibitors inducing apoptosis. Fut Med Chem. 2017 [ in press].
   Web of Science ®Google Scholar
• Khamaisie H, Sussan S, Tal M, Najajreh Y, Ruthardt M, Mahajna J Oleic acid is the active component in the mushroom Daedalea gibbosa inhibiting Bcr-Abl kinase autophosphorylation activity. Anticancer Res. 2011;31(1):177–183.
   PubMed Web of Science ®Google Scholar