Apoptosis-like death in bacteria induced by HAMLET, a human milk lipid-protein complex

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Hakansson, Anders P ^a,b   Roche Hakansson, Hazeline ^a   Mossberg, Ann Kristin ^c   Svanborg, Catharina ^c,d  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c LUND UNIVERSITY   (Sweden)

^d AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA LACTALBUMIN; HUMAN ALPHA LACTALBUMIN MADE LETHAL TO TUMOR CELLS PROTEIN; OLEIC ACID; SERINE PROTEINASE; UNCLASSIFIED DRUG; CALCIUM; DEOXYRIBONUCLEASE; HAMLET COMPLEX, HUMAN; LACTALBUMIN; N ACETYLMURAMOYLALANINE AMIDASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL CELL; BACTERIAL VIABILITY; BACTERIOLYSIS; CALCIUM TRANSPORT; CHROMATIN CONDENSATION; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA CLEAVAGE; DNA DEGRADATION; DNA FRAGMENTATION; ENZYME ACTIVITY; GEL ELECTROPHORESIS; HAEMOPHILUS INFLUENZAE; LEUKEMIA CELL LINE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION SWELLING; MOLECULAR WEIGHT; NONHUMAN; PROTEIN LIPID INTERACTION; RAT; STREPTOCOCCUS PNEUMONIAE; TUMOR CELL DESTRUCTION; CELL MEMBRANE; CHROMATIN; CYTOLOGY; DRUG EFFECT; HUMAN; METABOLISM; MICROBIOLOGICAL EXAMINATION; NEOPLASM; PATHOLOGY;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA; STREPTOCOCCUS PNEUMONIAE;

APOPTOSIS; CALCIUM; CELL MEMBRANE; CHROMATIN; DEOXYRIBONUCLEASES; DNA FRAGMENTATION; HAEMOPHILUS INFLUENZAE; HUMANS; JURKAT CELLS; LACTALBUMIN; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROBIAL SENSITIVITY TESTS; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; NEOPLASMS; OLEIC ACIDS; SERINE PROTEASES; STREPTOCOCCUS PNEUMONIAE;

EID: 79952546939     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017717     Document Type: Article

References (60)

1. Hakansson A, Zhivotovsky B, Orrenius S, Sabharwal H, Svanborg C, (1995) Apoptosis induced by a human milk protein. Proc Natl Acad Sci U S A 92: 8064-8068.
2. Svensson M, Hakansson A, Mossberg AK, Linse S, Svanborg C, (2000) Conversion of alpha-lactalbumin to a protein inducing apoptosis. Proc Natl Acad Sci U S A 97: 4221-4226.
3. Hakansson A, Svensson M, Mossberg AK, Sabharwal H, Linse S, et al. (2000) A folding variant of alpha-lactalbumin with bactericidal activity against Streptococcus pneumoniae. Mol Microbiol 35: 589-600.
4. Svensson M, Mossberg AK, Pettersson J, Linse S, 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.
5. Taylor RC, Cullen SP, Martin SJ, (2008) Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 9: 231-241.
6. Majno G, Joris I, (1995) Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146: 3-15.
7. Ameisen JC, (1996) The origin of programmed cell death. Science 272: 1278-1279.
8. Lewis K, (2000) Programmed death in bacteria. Microbiol Mol Biol Rev 64: 503-514.
9. Heine WE, Klein PD, Reeds PJ, (1991) The importance of alpha-lactalbumin in infant nutrition. J Nutr 121: 277-283.
10. Hakansson A, Roche H, Mirza S, McDaniel LS, Brooks-Walter A, et al. (2001) Characterization of binding of human lactoferrin to pneumococcal surface protein A. Infect Immun 69: 3372-3381.
11. Hammerschmidt S, Talay SR, Brandtzaeg P, Chhatwal GS, (1997) SpsA, a novel pneumococcal surface protein with specific binding to secretory immunoglobulin A and secretory component. Mol Microbiol 25: 1113-1124.
12. Dave S, Carmicle S, Hammerschmidt S, Pangburn MK, McDaniel LS, (2004) Dual roles of PspC, a surface protein of Streptococcus pneumoniae, in binding human secretory IgA and factor H. J Immunol 173: 471-477.
13. Anderton JM, Rajam G, Romero-Steiner S, Summer S, Kowalczyk AP, et al. (2007) E-cadherin is a receptor for the common protein pneumococcal surface adhesin A (PsaA) of Streptococcus pneumoniae. Microb Pathog 42: 225-236.
14. Campos MA, Vargas MA, Regueiro V, Llompart CM, Alberti S, et al. (2004) Capsule polysaccharide mediates bacterial resistance to antimicrobial peptides. Infect Immun 72: 7107-7114.
15. Tomasz A, Moreillon P, Pozzi G, (1988) Insertional inactivation of the major autolysin gene of Streptococcus pneumoniae. J Bacteriol 170: 5931-5934.
16. Tait SW, Green DR, (2008) Caspase-independent cell death: leaving the set without the final cut. Oncogene 27: 6452-6461.
17. Parrish JZ, Xue D, (2006) Cuts can kill: the roles of apoptotic nucleases in cell death and animal development. Chromosoma 115: 89-97.
18. Tettelin H, Nelson KE, Paulsen IT, Eisen JA, Read TD, et al. (2001) Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293: 498-506.
19. Claverys JP, Martin B, Polard P, (2009) The genetic transformation machinery: composition, localization, and mechanism. FEMS Microbiol Rev 33: 643-656.
20. Kohler C, Gogvadze V, Hakansson A, Svanborg C, Orrenius S, et al. (2001) A folding variant of human alpha-lactalbumin induces mitochondrial permeability transition in isolated mitochondria. Eur J Biochem 268: 186-191.
21. Kohler C, Hakansson A, Svanborg C, Orrenius S, Zhivotovsky B, (1999) Protease activation in apoptosis induced by MAL. Exp Cell Res 249: 260-268.
22. Gray MW, Burger G, Lang BF, (1999) Mitochondrial evolution. Science 283: 1476-1481.
23. Hallgren O, Gustafsson L, Irjala H, Selivanova G, Orrenius S, et al. (2006) HAMLET triggers apoptosis but tumor cell death is independent of caspases, Bcl-2 and p53. Apoptosis 11: 221-233.
24. Rammer P, Groth-Pedersen L, Kirkegaard T, Daugaard M, Rytter A, et al. (2010) BAMLET Activates a Lysosomal Cell Death Program in Cancer Cells. Mol Cancer Ther 9: 24-32.
25. Ankarcrona M, Zhivotovsky B, Holmstrom T, Diana A, Eriksson JE, et al. (1996) Lamin and beta tubulin fragmentation precede chromatin degradation in glutamate induced neuronal apoptosis. Neuroreport 7: 2659-2664.
26. Susin SA, Daugas E, Ravagnan L, Samejima K, Zamzami N, et al. (2000) Two distinct pathways leading to nuclear apoptosis. J Exp Med 192: 571-580.
27. Lemasters JJ, Theruvath TP, Zhong Z, Nieminen AL, (2009) Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta 1787: 1395-1401.
28. Giorgi C, Romagnoli A, Pinton P, Rizzuto R, (2008) Ca2+ signaling, mitochondria and cell death. Curr Mol Med 8: 119-130.
29. Pinton P, Giorgi C, Siviero R, Zecchini E, Rizzuto R, (2008) Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene 27: 6407-6418.
30. Crompton M, (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341: 233-249.
31. Kroemer G, Reed JC, (2000) Mitochondrial control of cell death. Nat Med 6: 513-519.
32. Dominguez DC, (2004) Calcium signalling in bacteria. Mol Microbiol 54: 291-297.
33. Norris V, Grant S, Freestone P, Canvin J, Sheikh FN, et al. (1996) Calcium signalling in bacteria. J Bacteriol 178: 3677-3682.
34. Trombe MC, Clave C, Manias JM, (1992) Calcium regulation of growth and differentiation in Streptococcus pneumoniae. J Gen Microbiol 138: 77-84.
35. Trombe MC, (1993) Characterization of a calcium porter of Streptococcus pneumoniae involved in calcium regulation of growth and competence. J Gen Microbiol 139: 433-439.
36. Bayles KW, (2007) The biological role of death and lysis in biofilm development. Nat Rev Microbiol 5: 721-726.
37. Claverys JP, Havarstein LS, (2007) Cannibalism and fratricide: mechanisms and raisons d'etre. Nat Rev Microbiol 5: 219-229.
38. Avery OT, MacLeod CM, McCarty M, (1944) Studies on the chemical nature of the substance inducing transformation of pneumococcal types. Induction of transformation by a dexoxyribonuceic acid fraction isolated from pneumococcus type III. J Exp Med 79: 137-158.
39. Lawrence RM, Pane CA, (2007) Human breast milk: current concepts of immunology and infectious diseases. Curr Probl Pediatr Adolesc Health Care 37: 7-36.
40. Davis MK, (1998) Review of the evidence for an association between infant feeding and childhood cancer. Int J Cancer Suppl 11 pp. 29-33.
41. Lindahl L, Vogel HJ, (1984) Metal-ion-dependent hydrophobic-interaction chromatography of a-lactalbumin. Analytical Biochemistry 140: 394-402.
42. Yother J, McDaniel LS, Briles DE, (1986) Transformation of encapsulated Streptococcus pneumoniae. J Bacteriol 168: 1463-1465.
43. Briles DE, Nahm M, Schroer K, Davie J, Baker P, et al. (1981) Antiphosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 streptococcus pneumoniae. J Exp Med 153: 694-705.
44. McDaniel LS, Sheffield JS, Swiatlo E, Yother J, Crain MJ, et al. (1992) Molecular localization of variable and conserved regions of pspA and identification of additional pspA homologous sequences in Streptococcus pneumoniae. Microb Pathog 13: 261-269.
45. Andersson B, Dahmen J, Frejd T, Leffler H, Magnusson G, et al. (1983) Identification of an active disaccharide unit of a glycoconjugate receptor for pneumococci attaching to human pharyngeal epithelial cells. J Exp Med 158: 559-570.
46. Andersson B, Eriksson B, Falsen E, Fogh A, Hanson L, et al. (1981) Adhesion of Streptococcus pneumoniae to human pharyngeal epithelial cells in vitro: Differences in adhesive capacity among strains isolated from subjects with otitis media, septicemia or meningitis or from healthy donors. Infect Immun 32: 311-317.
47. Briles DE, Hollingshead SK, King J, Swift A, Braun PA, et al. (2000) Immunization of humans with recombinant pneumococcal surface protein A (rPspA) elicits antibodies that passively protect mice from fatal infection with Streptococcus pneumoniae bearing heterologous PspA. J Infect Dis 182: 1694-1701.
48. Roche H, Hakansson A, Hollingshead SK, Briles DE, (2003) Regions of PspA/EF3296 best able to elicit protection against Streptococcus pneumoniae in a murine infection model. Infect Immun 71: 1033-1041.
49. Jorgensen JH, Doern GV, Ferraro MJ, Knapp CC, Swenson JM, et al. (1992) Multicenter evaluation of the use of Haemophilus test medium for broth microdilution antimicrobial susceptibility testing of Streptococcus pneumoniae and development of quality control limits. J Clin Microbiol 30: 961-966.
50. Berry AM, Lock RA, Hansman D, Paton JC, (1989) Contribution of autolysin to virulence of Streptococcus pneumoniae. Infect Immun 57: 2324-2330.
51. Yother J, Handsome GL, Briles DE, (1992) Truncated forms of PspA that are secreted from Streptococcus pneumoniae and their use in functional studies and cloning of the pspA gene. J Bacteriol 174: 610-618.
52. Balachandran P, Brooks-Walter A, Virolainen-Julkunen A, Hollingshead SK, Briles DE, (2002) Role of pneumococcal surface protein C in nasopharyngeal carriage and pneumonia and its ability to elicit protection against carriage of Streptococcus pneumoniae. Infect Immun 70: 2526-2534.
53. Berry AM, Paton JC, (1996) Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect Immun 64: 5255-5262.
54. Berry AM, Yother J, Briles DE, Hansman D, Paton JC, (1989) Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae. Infect Immun 57: 2037-2042.
55. Smith AW, Roche H, Trombe MC, Briles DE, Hakansson A, (2002) Characterization of the dihydrolipoamide dehydrogenase from Streptococcus pneumoniae and its role in pneumococcal infection. Mol Microbiol 44: 431-448.
56. Puyet A, Greenberg B, Lacks SA, (1989) The exoA gene of Streptococcus pneumoniae and its product, a DNA exonuclease with apurinic endonuclease activity. J Bacteriol 171: 2278-2286.
57. Puyet A, Greenberg B, Lacks SA, (1990) Genetic and structural characterization of endA. J Mol Biol 213: 727-738.
58. Campagnari AA, Gupta MR, Dudas KC, Murphy TF, Apicella MA, (1987) Antigenic diversity of lipooligosaccharides of nontypable Haemophilus influenzae. Infect Immun 55: 882-887.
59. Lysenko E, Richards JC, Cox AD, Stewart A, Martin A, et al. (2000) The position of phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae affects binding and sensitivity to C-reactive protein-mediated killing. Mol Microbiol 35: 234-245.
60. Alexander HE, Leidy G, (1951) Determination of inherited traits of H. influenzae by desoxyribonucleic acid fractions isolated from type-specific cells. J Exp Med 93: 345-359.