Oleic acid is a key cytotoxic component of HAMLET-like complexes

Biological Chemistry

Volumn 393, Issue 1-2, 2012, Pages 85-92

  Permyakov, Sergei E ^a,b   Knyazeva, Ekaterina L ^a   Khasanova, Leysan M ^a,b   Fadeev, Roman S ^c   Zhadan, Andrei P ^a   Roche Hakansson, Hazeline ^d   Håkansson, Anders P ^d,e   Akatov, Vladimir S ^c   Permyakov, Eugene A ^a,b  

^a INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

^b PUSHCHINO STATE UNIVERSITY   (Russian Federation)

^c INSTITUTE OF THEORETICAL AND EXPERIMENTAL BIOPHYSICS   (Russian Federation)

^d UNIVERSITY AT BUFFALO   (United States)

^e UNIVERSITY AT BUFFALO   (United States)

Author keywords

lactalbumin; lactoglobulin; Cytotoxicity; HAMLET; Oleic acid; Parvalbumin

Indexed keywords

ALPHA LACTALBUMIN; BETA LACTOGLOBULIN; CYTOTOXIC AGENT; HUMAN ALPHA LACTALBUMIN MADE LETHAL TO TUMOR CELL; OLEIC ACID; PARVALBUMIN; UNCLASSIFIED DRUG;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL OUTER MEMBRANE; CANCER CELL CULTURE; CELL DEATH; CELL VIABILITY; COLONY FORMING UNIT; COMPLEX FORMATION; CYTOTOXICITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IC 50; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; STREPTOCOCCUS PNEUMONIA; TUMOR CELL DESTRUCTION;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTINEOPLASTIC AGENTS; CATTLE; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; LACTALBUMIN; LACTOGLOBULINS; MICROBIAL SENSITIVITY TESTS; OLEIC ACID; PARVALBUMINS; PROTEIN STABILITY; STREPTOCOCCUS PNEUMONIAE; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPERATURE;

BOVINAE; STREPTOCOCCUS PNEUMONIAE;

EID: 84856173469     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC-2011-230     Document Type: Article

References (57)

1. Acharya, K.R., Stuart, D.I., Walker, N.P., Lewis, M., and Phillips, D.C. (1989). Refined structure of baboon alpha-lactalbumin at 1.7 A resolution. Comparison with C-type lysozyme. J. Mol. Biol. 208, 99-127. (Pubitemid 19191520)
2. Argiris, K., Panethymitaki, C., and Tavassoli, M. (2011). Naturally occurring, tumor-specific, therapeutic proteins. Exp. Biol. Med. 236, 524-536.
3. Arndt-Jovin, D.J. and Jovin, T.M. (1989). Fluorescence labeling and microscopy of DNA. Methods Cell Biol. 30, 417-448.
4. Barbiroli, A., Bonomi, F., Ferranti, P., Fessas, D., Nasi, A., Rasmussen, P., and Iametti, S. (2011). Bound fatty acids modulate the sensitivity of bovine beta-lactoglobulin to chemical and physical denaturation. J. Agric. Food. Chem. 59, 5729-5737.
5. Brinkmann, C.R., Heegaard, C.W., Petersen, T.E., Jensenius, J.C., and Thiel, S. (2011). The toxicity of bovine alpha-lactalbumin made lethal to tumor cells is highly dependent on oleic acid and induces killing in cancer cell lines and noncancer-derived primary cells. FEBS J. 278, 1955 - 1967.
6. Casbarra, A., Birolo, L., Infusini, G., Dal Piaz, F., Svensson, M., Pucci, P., Svanborg, C., and Marino, G. (2004). Conformational analysis of HAMLET, the folding variant of human alpha-lactalbumin associated with apoptosis. Protein Sci. 13, 1322-1330. (Pubitemid 38526097)
7. Cistola, D.P., Hamilton, J.A., Jackson, D., and Small, D.M. (1988). Ionization and phase behavior of fatty acids in water: application of the Gibbs phase rule. Biochemistry 27, 1881-1888.
8. Cury-Boaventura, M.F., Pompeia, C., and Curi, R. (2004). Comparative toxicity of oleic acid and linoleic acid on Jurkat cells. Clin. Nutr. 23, 721-732. (Pubitemid 39107053)
9. Duringer, C., Hamiche, A., Gustafsson, L., Kimura, H., and Svanborg, C. (2003). HAMLET interacts with histones and chromatin in tumor cell nuclei. J. Biol. Chem. 278, 42131-42135. (Pubitemid 37310480)
10. Edwards, K., Silvander, M., and Karlsson, G. (1995). Aggregate structure in dilute aqueous dispersions of oleic acid/sodium oleate and oleic acid/sodium oleate/egg phosphatidylcholine. Langmuir 11, 2429-2434.
11. Epps, D.E., Wolfe, M.L., and Groppi, V. (1994). Characterization of the steady-state and dynamic fluorescence properties of the potential-sensitive dye bis-(1,3-dibutylbarbituric acid)trimethine oxonol (Dibac4(3)) in model systems and cells. Chem. Phys. Lipids 69, 137-150.
12. Fang, R., Jing, H., Chai, Z., Zhao, G., Stoll, S., Ren, F., Liu, F., and Leng, X. (2011). Design and characterization of protein-quercetin bioactive nanoparticles. J. Nanobiotechnol. 9, 19.
13. Fauser, J.K., Prisciandaro, L.D., Cummins, A.G., and Howarth, G.S. (2011). Fatty acids as potential adjunctive colorectal chemotherapeutic agents. Cancer Biol. Ther. 11, 724-731.
14. Fischer, W., Gustafsson, L., Mossberg, A.K., Gronli, J., Mork, S., Bjerkvig, R., and Svanborg, C. (2004). 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. 64, 2105-2012.
15. Fukuda, H., Goto, A., Yoshioka, H., Goto, R., Morigaki, K., and Walde, P. (2001). Electron spin resonance study of the pHinduced transformation of micelles to vesicles in an aqueous oleic acid/oleate system. Langmuir 17, 4223-4231. (Pubitemid 35330287)
16. Gustafsson, L., Leijonhufvud, I., Aronsson, A., Mossberg, A.K., and Svanborg, C. (2004). Treatment of skin papillomas with topical alpha-lactalbumin-oleic acid. N. Engl. J. Med. 350, 2663-2672.
17. Gustafsson, L., Aits, S., Onnerfjord, P., Trulsson, M., Storm, P., and Svanborg, C. (2009). Changes in proteasome structure and function caused by HAMLET in tumor cells. PLoS One 4, e5229.
18. Hakansson, A., Svensson, M., Mossberg, A.K., Sabharwal, H., Linse, S., Lazou, I., Lonnerdal, B., and Svanborg, C. (2000). A folding variant of alpha-lactalbumin with bactericidal activity against Streptococcus pneumoniae. Mol. Microbiol. 35, 589-600. (Pubitemid 30085276)
19. Hakansson, A.P., Roche-Hakansson, H., Mossberg, A.K., and Svanborg, C. (2011). Apoptosis-like death in bacteria induced by HAMLET, a human milk lipid-protein complex. PLoS One 10, e17717.
20. Hussain, R. and Siligardi, G. (2010). Novel drug delivery system for lipophilic therapeutics of small molecule, peptide-based and protein drugs. Chirality 22, 44-46.
21. Jiang, H.R. and Liu, N. (2010). Self-assembled beta- lactoglobulinconjugated linoleic acid complex for colon cancer-targeted substance. J. Dairy Sci. 93, 3931-3939.
22. Kaplanas, R.I. and Antanavichyus, A.I. (1975). Isolation and purification of a-lactalbumin, a component of lactose synthetase. Biochemistry (Mosc.) 40, 493-495.
23. Knyazeva, E.L., Grishchenko, V.M., Fadeev, R.S., Akatov, V.S., Permyakov, S.E., and Permyakov, E.A. (2008). Who is Mr. HAMLET? Interaction of human a-lactalbumin with monomeric oleic acid. Biochemistry 47, 13127-13137.
24. Kontopidis, G., Holt, C., and Sawyer, L. (2004). Invited review: beta-lactoglobulin: binding properties, structure, and function. J. Dairy Sci. 87, 785-796. (Pubitemid 44151704)
25. Kretsinger, R.H. and Nockolds, C.E. (1973). Carp muscle calciumbinding protein. II. Structure determination and general description. J. Biol. Chem. 248, 3313-3326.
26. Lindahl, L. and Vogel, H.J. (1984). Metal-ion-dependent hydrophobic- interaction chromatography of alpha-lactalbumins. Anal Biochem 140, 394-402. (Pubitemid 14071950)
27. Mok, K.H., Pettersson, J., Orrenius, S., and Svanborg, C. (2007). HAMLET, protein folding, and tumor cell death. Biochem. Biophys. Res. Commun. 354, 1-7. (Pubitemid 46123199)
28. Mossberg, A.K., Hou, Y., Svensson, M., Holmqvist, B., and Svanborg, C. (2010a). HAMLET treatment delays bladder cancer development. J. Urol. 183, 1590-1597.
29. Mossberg, A.K., Hun Mok, K., Morozova-Roche, L.A., and Svanborg, C. (2010b). Structure and function of human alpha-lactalbumin made lethal to tumor cells (HAMLET)-type complexes. FEBS J. 277, 4614-4625.
30. Mossberg, A.K., Puchades, M., Halskau, O., Baumann, A., Lanekoff, I., Chao, Y.X., Martinez, A., Svanborg, C., and Karlsson, R. (2010c). HAMLET interacts with lipid membranes and perturbs their structure and integrity. PLoS One 5, e9384.
31. Nielsen, S.B., Wilhelm, K., Vad, B., Schleucher, J., Morozova-Roche, L.A., and Otzen, D. (2010). The interaction of equine lysozyme: oleic acid complexes with lipid membranes suggests a cargo offloading mechanism. J. Mol. Biol. 398, 351-361.
32. Nockolds, C.E., Kretsinger, R.H., Coffee, C.J., and Bradshaw, R.A. (1972). Structure of a calcium-binding carp myogen. Proc. Natl. Acad. Sci. USA 69, 581-584.
33. Noteborn, M.H. (2009). Proteins selectively killing tumor cells. Eur. J. Pharmacol. 625, 165-173.
34. Nozaka, M., Kuwajima, K., Nitta, K., and Sugai, S. (1978). Detection and characterization of the intermediate on the folding pathway of human a-lactalbumin. Biochemistry 17, 3753-3758. (Pubitemid 9022585)
35. Pace, C.N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995). How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4, 2411-2423.
36. Perez, M.D. and Calvo, M. (1995). Interaction of beta-lactoglobulin with retinol and fatty acids and its role as a possible biological function for this protein: a review. J. Dairy Sci. 78, 978-988.
37. Perez, M.D., Diaz de Villegas, C., Sanchez, L., Aranda, P., Ena, J.M., and Calvo, M. (1989). Interaction of fatty acids with betalactoglobulin and albumin from ruminant milk. J. Biochem. 106, 1094-1097. (Pubitemid 20010127)
38. Permyakov, E. (2007). Parvalbumin (New York, NY, USA: Nova Science).
39. Permyakov, E.A. (1993). Luminescent Spectroscopy of Proteins. (Boca Raton, FL, USA: CRC Press).
40. Permyakov, E.A. (2005). a-Lactalbumin (New York, NY, USA: Nova Science).
41. Permyakov, S.E., Bakunts, A.G., Permyakova, M.E., Denesyuk, A.I., Uversky, V.N., and Permyakov, E.A. (2009a). Metal-controlled interdomain cooperativity in parvalbumins. Cell Calcium 46, 163-275.
42. Permyakov, S.E., Karnoup, A.S., Bakunts, A.G., and Permyakov, E.A. (2009b). Sequence microheterogeneity of parvalbumin pI 5.0 of pike: a mass spectrometric study. Biochim. Biophys. Acta 1794, 129-136.
43. Permyakov, S.E., Knyazeva, E.L., Leonteva, M.V., Fadeev, R.S., Chekanov, A.V., Zhadan, A.P., Hakansson, A.P., Akatov, V.S., and Permyakov, E.A. (2011). A novel method for preparation of HAMLET-like protein complexes. Biochimie 93, 1495-1501.
44. Pettersson, J., Mossberg, A.K., and Svanborg, C. (2006). alpha- Lactalbumin species variation, HAMLET formation, and tumor cell death. Biochem. Biophys. Res. Commun. 345, 260-270.
45. Pettersson-Kastberg, J., Mossberg, A.K., Trulsson, M., Yong, Y.J., Min, S., Lim, Y., O'Brien, J.E., Svanborg, C., and Mok, K.H. (2009). alpha-Lactalbumin, engineered to be nonnative and inactive, kills tumor cells when in complex with oleic acid: a new biological function resulting from partial unfolding. J. Mol. Biol. 394, 994-1010.
46. Puyol, P., Perez, D.M., Peiro, J.M., and Calvo, M. (1994). Effect of binding of retinol and palmitic acid to bovine b-lactoglobulin on its resistance to thermal denaturation. J. Dairy Sci. 77, 1494-1502.
47. Rao, K.S. and Gerday, C. (1973). Low molecular weight proteins of pike (esox lucius) white muscles. II. Chemical and physical properties. Comp. Biochem. Physiol. B 44, 1113-1125.
48. Spolaore, B., Pinato, O., Canton, M., Zambonin, M., Polverino de Laureto, P., and Fontana, A. (2010). alpha-Lactalbumin forms with oleic acid a high molecular weight complex displaying cytotoxic activity. Biochemistry 49, 8658-8667.
49. Svanborg, C., Agerstam, H., Aronson, A., Bjerkvig, R., Duringer, C., Fischer, W., Gustafsson, L., Hallgren, O., Leijonhuvud, I., Linse, S., et al. (2003). HAMLET kills tumor cells by an apoptosis-like mechanism - cellular, molecular, and therapeutic aspects. Adv. Cancer Res. 88, 1-29. (Pubitemid 36343277)
50. Svensson, M., Hakansson, A., Mossberg, A.K., Linse, S., and Svanborg, C. (2000). Conversion of alpha-lactalbumin to a protein inducing apoptosis. Proc. Natl. Acad. Sci. USA 97, 4221-4226. (Pubitemid 30226114)
51. Svensson, M., Mossberg, A.K., Pettersson, J., Linse, S., and Svanborg, C. (2003). Lipids as cofactors in protein folding: stereo-specific lipid-protein interactions are required to form HAMLET (human alpha-lactalbumin made lethal to tumor cells). Protein Sci. 12, 2805-2814. (Pubitemid 37445104)
52. Tolin, S., De Franceschi, G., Spolaore, B., Frare, E., Canton, M., Polverino de Laureto, P., and Fontana, A. (2010). The oleic acid complexes of proteolytic fragments of alpha-lactalbumin display apoptotic activity. FEBS J. 277, 163-173.
53. Trulsson, M., Yu, H., Gisselsson, L., Chao, Y., Urbano, A., Aits, S., Mossberg, A.K., and Svanborg, C. (2011). HAMLET binding to alpha-actinin facilitates tumor cell detachment. PLoS One 6, e17179.
54. Vukojevic, V., Bowen, A.M., Wilhelm, K., Ming, Y., Ce, Z., Schleucher, J., Hore, P.J., Terenius, L., and Morozova-Roche, L.A. (2010). Lipoprotein complex of equine lysozyme with oleic acid (ELOA) interactions with the plasma membrane of live cells. Langmuir 26, 14782-14787.
55. Wilhelm, K., Darinskas, A., Noppe, W., Duchardt, E., Mok, K.H., Vukojevic, V., Schleucher, J., and Morozova-Roche, L.A. (2009). Protein oligomerization induced by oleic acid at the solid-liquid interface - equine lysozyme cytotoxic complexes. FEBS J 276, 3975-3989.
56. Zherelova, O.M., Kataev, A.A., Grishchenko, V.M., Knyazeva, E.L., Permyakov, S.E., and Permyakov, E.A. (2009). Interaction of antitumor alpha-lactalbumin-oleic acid complexes with artificial and natural membranes. J. Bioenerg. Biomembr. 41, 229-237.
57. Zhu, Y., Schwarz, S., Ahlemeyer, B., Grzeschik, S., Klumpp, S., and Krieglstein, J. (2005). Oleic acid causes apoptosis and dephosphorylates Bad. Neurochem. Int. 46, 127-135. (Pubitemid 41556620)