Oleic acid complex of bovine α-lactalbumin induces eryptosis in human and other erythrocytes by a Ca2 +-independent mechanism

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 9, 2015, Pages 1729-1739

  Hoque, Mehboob ^a   Nanduri, Ravikanth ^b   Gupta, Jyoti ^a   Mahajan, Sahil ^b   Gupta, Pawan ^b   Saleemuddin, M ^a  

^a ALIGARH MUSLIM UNIVERSITY   (India)

^b INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

Author keywords

a Lactalbumin; Antitumor drugs; Eryptosis; HAMLET BAMLET; Oleic acid

Indexed keywords

ACETYLCYSTEINE; ALPHA LACTALBUMIN; AMILORIDE; BARIUM CHLORIDE; BOVINE ALPHA LACTALBUMIN MADE LETHAL TO TUMOR CELLS; CALCEIN; CALCIUM ION; CYSTEINE PROTEINASE INHIBITOR; HEMOGLOBIN; OLEIC ACID; PHOSPHATIDYLSERINE; SPHINGOMYELIN PHOSPHODIESTERASE INHIBITOR; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL BLOCKING AGENT; CALCIUM; LACTALBUMIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL TRANSFORMATION; CHICKEN; CONTROLLED STUDY; ECHINOCYTE; ERYPTOSIS; ERYTHROCYTE; GOAT; HEMOLYSIS; HUMAN; HUMAN CELL; LIPID COMPOSITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; REGULATORY MECHANISM; ANIMAL; BOVINE; DRUG EFFECTS;

BOVINAE; CAPRA HIRCUS;

AMILORIDE; ANIMALS; CALCIUM; CATTLE; CHICKENS; ERYTHROCYTES; GOATS; HEMOLYSIS; HUMANS; LACTALBUMIN; OLEIC ACIDS;

EID: 84930643432     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2015.04.009     Document Type: Article

References (75)

1. K. Alzoubi, S. Calabro, C. Faggio, and F. Lang Stimulation of suicidal erythrocyte death by sulforaphane Basic Clin Pharmacol Toxicol 116 2015 229 235
2. X. An, M. Salomao, X. Guo, W. Gratzer, and N. Mohandas Tropomyosin modulates erythrocyte membrane stability Blood 109 2007 1284 1288
3. C.P. Berg, I.H. Engels, A. Rothbart, K. Lauber, A. Renz, and S.F. Schlosser Human mature red blood cells express caspase-3 and caspase-8, but are devoid of mitochondrial regulators of apoptosis Cell Death Diff 8 2001 1197 1206
4. A. Bogdanova, A. Makhro, J. Wang, P. Lipp, and L. Kaestner Calcium in red blood cells - a perilous balance Int J Mol Sci 14 2013 9848 9872
5. D. Bratosin, J. Estaquier, F. Petit, D. Arnoult, B. Quatannens, and J.P. Tissier Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria Cell Death Diff 8 2001 1143 1156
6. C.R. Brinkmann, C.W. Heegaard, T.E. Petersen, J.C. Jensenius, and S. Thiel 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 2011 1955 1967
7. C.R. Brinkmann, S. Thiel, M.K. Larsen, T.E. Petersen, J.C. Jensenius, and C.W. Heegaard Preparation and comparison of cytotoxic complexes formed between oleic acid and either bovine or human α-lactalbumin J Dairy Sci 94 2011 2159 2170
8. A. Csordas, and M. Rybczynska Critical temperatures for the interaction of free fatty acids with the erythrocyte membrane Biochim Biophys Acta 944 1988 155 163
9. E. Daugas, C. Cande, and G. Kroemer Erythrocytes: death of a mummy Cell Death Diff 8 2001 1131 1133
10. B. Deuticke Transformation and restoration of biconcave shape of human erythrocytes induced by amphiphilic agents and changes of ionic environment Biochim Biophys Acta 163 1968 494 500
11. C. Duringer, E. Hamiche, L. Gustafsson, H. Kimura, and C. Svanborg HAMLET interacts with histones and chromatin in tumor cell nuclei J Biol Chem 278 2003 42131 42135
12. B. Fang, M. Zhang, M. Tian, L. Jiang, H.Y. Guo, and F.Z. Ren Bovine lactoferrin binds oleic acid to form an anti-tumor complex similar to HAMLET Biochim Biophys Acta 1841 2014 535 543
13. V.R. Fantin, M.J. Berardi, L. Scorrano, S.J. Korsmeyer, and P. Leder A novel mitochondriotoxic small molecule that selectively inhibits tumor cell growth Cancer Cell 2 2002 29 42
14. W. Fischer, L. Gustafsson, A.K. Mossberg, J. Gronli, S. Mork, and R. Bjerkvig 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 2004 2105 2112
15. A. Fontana, B. Spolaore, and P. Polverino de Laureto The biological activities of protein/oleic acid complexes reside in the fatty acid Biochim Biophys Acta 1834 2013 1125 1143
16. M. Gao, P.M. Lau, and S.K. Kong Mitochondrial toxin betulinic acid induces in vitro eryptosis in human red blood cells through membrane permeabilization Arch Toxicol 88 2014 755 768
17. M. Gao, S.Y. Wong, P.M. Lau, and S.K. Kong Ferutinin induces in vitro eryptosis/erythroptosis in human erythrocytes through membrane permeabilization and calcium influx Chem Res Toxicol 26 2013 1218 1228
18. 2 + rise and membrane permeabilization Arch Toxicol 86 2012 741 752
19. T. George, N.J. Bal, and S. Krishnamurthy Studies on hemolysis of human erythrocytes by linoleic acid J Biosci 1 1979 385 392
20. L. Gustafsson, I. Leijonhufvud, A. Aronsson, A.K. Mossberg, and C. Svanborg Treatment of skin papillomas with topical alpha-lactalbumin-oleic acid New Eng J Med 350 2004 2663 2672
21. A.P. Hakansson, H. Rochje-Hakansson, A.K. Mossberg, and C. Svanborg Apoptosis-like cell death in bacteria induced by HAMLET, a human milk lipid-protein complex PLoS ONE 6 3 2011 e17717
22. A. Hakansson, J. Andreasson, B. Zhivotovsky, D. Karpman, S. Orrenius, and C. Svanborg Multimeric alpha-lactalbumin from human milk induces apoptosis through a direct effect on cell nuclei Exp Cell Res 246 1999 451 460
23. A. Hakansson, B. Zhivotovsky, S. Orrenius, H. Sabharwal, and C. Svanborg Apoptosis induced by a human milk protein Proc Natl Acad Sci, USA 92 1995 8064 8068
24. O. Hallgren, S. Aits, P. Brest, L. Gustafsson, A.K. Mossberg, and B. Wullt Apoptosis and tumor cell death in response to HAMLET (Human α-Lactalbumin Made Lethal to Tumor Cells). Bioactive components of milk Adv Exp Med Biol 606 2008 217 240
25. O. Hallgren, L. Gustafsson, H. Irjala, G. Selivanova, S. Orrenius, and C. Svanborg HAMLET triggers apoptosis but tumor cell death is independent of caspases, Bcl-2 and p53 Apoptosis 11 2006 221 233
26. J.C. Ho, P. Storm, A. Rydstrom, B. Bowen, F. Alsin, and L. Sullivan Lipids as tumoricidal components of human alpha-lactalbumin made lethal to tumor cells (HAMLET): unique and shared effects on signaling and death J Biol Chem 288 2013 17460 17471
27. C.S.J. Ho, A. Rydstrom, M. Trulsson, J. Balfors, P. Storm, and M. Puthia HAMLET: functional properties and therapeutic potential Future Oncol 8 2012 1301 1313
28. J. Ho, H. Sielaff, A. Nadeem, C. Svanborg, and G. Grüber The molecular motor F-ATP synthase is targeted by the tumoricidal protein HAMLET J Mol Biol 2015 10.1016/j.jmb.2015.01.024
29. M. Hoque, S. Dave, P. Gupta, and M. Saleemuddin Oleic acid may be the key contributor in the BAMLET-induced erythrocyte hemolysis and tumoricidal action PLoS ONE 8 2013 e68390
30. K. Jilani, and F. Lang Carmustine-induced phosphatidylserine translocation in the erythrocyte membrane Toxins 5 2013 703 716
31. T. Kamijima, A. Ohmura, T. Sato, K. Akimoto, M. Itabashi, and M. Mizuguchi Heat-treatment method for producing fatty acid-bound alpha-lactalbumin that induces tumor cell death Biochem Biophys Res Commun 376 2008 211 214
32. 2 +-mediated processes in goat erythrocytes Biochim Biophys Acta. 940 1988 165 169
33. H. Kleinig, H. Zentgraf, P. Comes, and J. Stadler Nuclear membranes and plasma membranes from hen erythrocytes. II. Lipid composition J BiolChem 246 1971 2996 3000
34. E.L. Knyazeva, V.M. Grishchenko, R.S. Fadeev, V.S. Akatov, S.E. Permyakov, and E.A. Permyakov Who is Mr. HAMLET? Interaction of human alpha-lactalbumin with monomeric oleic acid Biochemistry 47 2008 13127 13137
35. C. Kohler, V. Gogvadze, A. Hakansson, C. Svanborg, S. Orrenius, and B. Zhivotovsky A folding variant of human alpha-lactalbumin induces mitochondrial permeability transition in isolated mitochondria Eur J Biochem 268 2001 186 191
36. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
37. F. Lang, and S.M. Qadri Mechanisms and significance of eryptosis, the suicidal death of erythrocytes Blood Purif 33 2012 125 130
38. E. Lang, S.M. Qadri, and F. Lang Killing me softly - suicidal erythrocyte death Int J Biochem Cell Biol 44 2012 1236 1243
39. F. Lang, E. Lang, and M. Foller Physiology and pathophysiology of eryptosis Transfus Med Hemother. 39 2012 308 314
40. F. Lang, E. Gulbins, H. Lerche, S.M. Huber, D.S. Kempe, and M. Foller Eryptosis, a window to systemic disease. Cellular physiology and biochemistry Int J Exp Cell Physiol Biochem Pharmacol. 22 2008 373 380
41. F. Lang, K.S. Lang, P.A. Lang, S.M. Huber, and T. Wieder Mechanisms and significance of eryptosis Antioxid Redox Signal 8 2006 1183 1192
42. K.S. Lang, S. Myssina, V. Brand, C. Sandu, P.A. Lang, and S. Berchtold Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes Cell Death Diff 11 2004 231 243
43. K.S. Lang, C. Duranton, H. Poehlmann, S. Myssina, C. Bauer, and F. Lang Cation channels trigger apoptotic death of erythrocytes Cell Death Diff 10 2003 249 256
44. R.K.Y. Lee, R.C.Y. Ong, J.Y.N. Cheung, Y.C. Li, J.Y.W. Chan, and M.M.S. Lee Polyphyllin D - a potential anti-cancer agent to kill hepatocarcinoma cells with multi-drug resistance Curr Chem Biol 3 2009 409 419
45. H. Mahmud, M. Foller, and F. Lang Suicidal erythrocyte death triggered by cisplatin Toxicology 249 2008 40 44
46. D. Mandal, V. Baudin-Creuza, A. Bhattacharyya, S. Pathak, J. Delaunay, and M. Kundu Caspase 3-mediated proteolysis of the N-terminal cytoplasmic domain of the human erythroid anion exchanger 1 (band 3) J Biol Chem 278 2003 52551 52558
47. D. Mandal, P.K. Moitra, S. Saha, and J. Basu Caspase 3 regulates phosphatidylserine externalization and phagocytosis of oxidatively stressed erythrocytes FEBS Lett 513 2002 184 188
48. W.F. McPhedran On the hemolytic properties of fatty acids and their relation to the causation of toxic hemolysis and pernicious anemia J Exp Med 18 1913 527 542
49. D.J. Mitchell, B.G. McClure, and T.R. Tubman Simultaneous monitoring of gastric and oesophageal pH reveals limitations of conventional oesophageal pH monitoring in milk fed infants Arch Dis Child 84 2001 273 276
50. A.K. Mossberg, K.H. Mok, L.A. Morozova-Roche, and C. Svanborg Structure and function of human alpha-lactalbumin made lethal to tumor cells (HAMLET)-type complexes FEBS J 277 2010 4614 4625
51. A.K. Mossberg, M. Puchades, O. Halskau, A. Baumann, I. Lanekoff, and Y. Chao HAMLET interacts with lipid membranes and perturbs their structure and integrity PLoS ONE 5 2010 e9384
52. A.K. Mossberg, B. Wullt, L. Gustafsson, W. Mansson, E. Ljunggren, and C. Svanborg Bladder cancers respond to intravesical instillation of HAMLET (human alpha-lactalbumin made lethal to tumor cells) Int J Cancer 121 2007 1352 1359
53. F.B. Mullauer, J.H. Kessler, and J.P. Medema Betulinic acid, a natural compound with potent anticancer effects Anticancer Drugs 21 2010 215 227
54. T. Nakamura, T. Aizawa, R. Kariya, S. Okada, M. Demura, and K. Kawano Molecular mechanisms of the cytotoxicity of human alpha-lactalbumin made lethal to tumor cells (HAMLET) and other protein-oleic acid complexes J Biol Chem 288 2013 14408 14416
55. G.J. Nelson Lipid composition of erythrocytes in various mammalian species Biochim Biophys Acta 144 1967 221 232
56. E.L. Nemashkalova, A.S. Kazakov, L.M. Khasanova, E.A. Permyakov, and S.E. Permyakov Structural characterization of more potent alternatives to HAMLET, a tumoricidal complex of alpha-lactalbumin and oleic acid Biochemistry 52 2013 6286 6299
57. M. Puthia, P. Storm, A. Nadeem, S. Hsiung, and C. Svanborg Prevention and treatment of colon cancer by peroral administration of HAMLET (human alpha-lactalbumin made lethal to tumour cells) Gut 63 2014 131 142
58. P. Rammer, L. Groth-Pedersen, T. Kirkegaard, M. Daugaard, A. Rytter, and P. Szyniarowski BAMLET activates a lysosomal cell death program in cancer cells Mol. Cancer Ther. 9 2010 24 32
59. M.G. Rumsby, S. Sparrow, and C. Little The oleic acid-induced shape transformation of human erythrocytes [proceedings] Biochem Soc Trans 7 1979 922 924
60. M.P. Sheetz, and S.J. Singer Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions Proc Natl Acad Sci, U S A 71 11 1974 4457 4461
61. N. Sinevici, N. Harte, K.H. Mok, Y. Xie, and J. O'Sullivian The novel use of BAMLET in the treatment of oral squamous cell carcinoma Eur J Cancer 50 Suppl. 5 2014 S 310
62. J.L. Spivak, P. Gascon, and H. Ludwig Anemia management in oncology and hematology Oncologist 14 Suppl. 1 2009 43 56
63. B. Spolaore, O. Pinato, M. Canton, M. Zambonin, P. Polverino de Laureto, and A. Fontana Alpha-lactalbumin forms with oleic acid a high molecular weight complex displaying cytotoxic activity Biochemistry 49 2010 8658 8667
64. P. Storm, M.K. Puthia, S. Aits, A. Urbano, T. Northen, and S. Powers Conserved features of cancer cells define their sensitivity of HAMLET-induced death; c-Myc and glycolysis Oncogene 30 2011 4765 4779
65. P. Storm, T.K. Klausen, M. Trulsson, C.S.J. Ho, M. Dosnon, and T. Westergren A unifying mechanism for cancer cell death through ion channel activation by HAMLET PLoS ONE 8 2013 e58578
66. L.M. Sullivan, K.H. Mok, and A. Brodkorb The formation of an anti-cancer complex under simulated gastric conditions Food Digestion 7-18 2013
67. M. Svensson, A. Hakansson, S. Linse, A.K. Mossberg, and C. Svanborg Conversion of alpha-lactalbumin to a protein inducing apoptosis Proc Natl Acad Sci, USA 97 2000 4221 4226
68. P.L. Toogood Mitochondrial drugs Curr Opin Chem Biol 12 2008 457 463
69. 2 + pump ATPase: preliminary results of a species comparison Prog Clin Biol Res 55 1981 363 383
70. D.M. Vota, R.E. Maltaneri, S.D. Wenker, A.B. Nesse, and D.C. Vittori Differential erythropoietin action upon cells induced to eryptosis by different agents Cell Biochem Biophys 65 2013 145 157
71. E. Ward, R. Smith, J.J.V. Branca, D. Noakes, G. Morucci, and L. Thyer Clinical experience of cancer immunotherapy integrated with oleic acid complexed with de-glycosylated vitamin D binding protein Am J Immunol 2 2014 23 32
72. H. Wen, W.R. Glomm, and O. Halskau Cytotoxicity of bovine alpha-lactalbumin: oleic acid complexes correlates with the disruption of lipid membranes Biochim Biophys Acta 1828 2013 2691 2699
73. Y. Xie, N.P. Min, H. Harte, J.E. Kirk, H.P. O'Brien, and C. Voorheis Electrostatic interactions play an essential role in the binding of opleic acid with α-lactalbumin in the HAMLET-like complex: a study using charge-specific chemical modification Proteins 81 2013 1 17
74. O.M. Zherelova, A.A. Kataev, V.M. Grishchenko, E.L. Knyazeva, S.E. Permyakov, and E.A. Permyakov Interaction of antitumor alpha-lactalbumin-oleic acid complexes with artificial and natural membranes J Bioenerg Biomembr 41 2009 229 237
75. L. Zolla, and A. D'Alessandro An efficient apparatus for rapid deoxygenation of erythrocyte concentrates for alternative banking strategies J Blood Transfus 2013 2013 896537