HAMLET binding to α-actinin facilitates tumor cell detachment

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Trulsson, Maria ^a   Yu, Hao ^a   Gisselsson, Lennart ^b   Chao, Yinxia ^c   Urbano, Alexander ^c   Aits, Sonja ^a   Mossberg, Ann Kristin ^a   Svanborg, Catharina ^a  

^a LUND UNIVERSITY   (Sweden)

^b Phase Holographic Imaging AB   (Sweden)

^c AGENCY FOR SCIENCE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; ALPHA ACTININ 1; ALPHA ACTININ 4; ALPHA LACTALBUMIN; BETA1 INTEGRIN; F ACTIN; FOCAL ADHESION KINASE 1; HUMAN ALPHA LACTALBUMIN MADE LETHAL TO TUMOR CELL; ION CHANNEL; MITOGEN ACTIVATED PROTEIN KINASE 1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ACTIN; ACTININ; CELL EXTRACT; FOCAL ADHESION KINASE; HAMLET COMPLEX, HUMAN; LACTALBUMIN; OLEIC ACID; PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CELL ADHESION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; MOLECULAR MECHANICS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR CELL; BIOLOGICAL MODEL; CELL DEATH; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; NEOPLASM; PATHOLOGY; PROTEIN ANALYSIS; PROTEIN TRANSPORT; TUMOR CELL LINE;

ACTININ; ACTINS; AMINO ACID SEQUENCE; ANTIGENS, CD29; BINDING SITES; CELL ADHESION; CELL DEATH; CELL EXTRACTS; CELL LINE, TUMOR; CELL SURVIVAL; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; LACTALBUMIN; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEOPLASMS; OLEIC ACIDS; PEPTIDES; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 79952479246     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017179     Document Type: Article

References (56)

1. Grossmann J, (2002) Molecular mechanisms of "detachment-induced apoptosis-Anoikis". Apoptosis 7: 247-260.
2. Martin SS, Vuori K, (2004) Regulation of Bcl-2 proteins during anoikis and amorphosis. Biochim Biophys Acta 1692: 145-157.
3. Zaidel-Bar R, Itzkovitz S, Ma'ayan A, Iyengar R, Geiger B, (2007) Functional atlas of the integrin adhesome. Nat Cell Biol 9: 858-867.
4. Geiger B, Bershadsky A, Pankov R, Yamada KM, (2001) Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat Rev Mol Cell Biol 2: 793-805.
5. Beauvais DM, Rapraeger AC, (2004) Syndecans in tumor cell adhesion and signaling. Reprod Biol Endocrinol 2: 3.
6. Franzot G, Sjoblom B, Gautel M, Djinovic Carugo K, (2005) The crystal structure of the actin binding domain from alpha-actinin in its closed conformation: structural insight into phospholipid regulation of alpha-actinin. J Mol Biol 348: 151-165.
7. Kelly DF, Taylor KA, (2005) Identification of the beta1-integrin bindingsite on alpha-actinin by cryoelectron microscopy. J Struct Biol 149: 290-302.
8. Gluck U, Kwiatkowski DJ, Ben-Ze'ev A, (1993) Suppression of tumorigenicity in simian virus 40-transformed 3T3 cells transfected with alpha-actinin cDNA. Proc Natl Acad Sci U S A 90: 383-387.
9. Honda K, Yamada T, Endo R, Ino Y, Gotoh M, et al. (1998) Actinin-4, a novel actin-bundling protein associated with cell motility and cancer invasion. J Cell Biol 140: 1383-1393.
10. Otey CA, Vasquez GB, Burridge K, Erickson BW, (1993) Mapping of the alpha-actinin binding site within the beta 1 integrin cytoplasmic domain. J Biol Chem 268: 21193-21197.
11. Beggs AH, Byers TJ, Knoll JH, Boyce FM, Bruns GA, et al. (1992) Cloning and characterization of two human skeletal muscle alpha-actinin genes located on chromosomes 1 and 11. J Biol Chem 267: 9281-9288.
12. Gonzalez AM, Otey C, Edlund M, Jones JC, (2001) Interactions of a hemidesmosome component and actinin family members. J Cell Sci 114: 4197-4206.
13. Otey CA, Carpen O, (2004) Alpha-actinin revisited: a fresh look at an old player. Cell Motil Cytoskeleton 58: 104-111.
14. Dandapani SV, Sugimoto H, Matthews BD, Kolb RJ, Sinha S, et al. (2007) {alpha}-Actinin-4 Is Required for Normal Podocyte Adhesion. J Biol Chem 282: 467-477.
15. Quick Q, Skalli O, (2010) Alpha-actinin 1 and alpha-actinin 4: contrasting roles in the survival, motility, and RhoA signaling of astrocytoma cells. Exp Cell Res 316: 1137-1147.
16. Sjoblom B, Salmazo A, Djinovic-Carugo K, (2008) Alpha-actinin structure and regulation. Cell Mol Life Sci 65: 2688-2701.
17. 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.
18. 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.
19. Svanborg C, Agerstam H, Aronson A, Bjerkvig R, Duringer C, et al. (2003) HAMLET kills tumor cells by an apoptosis-like mechanism-cellular, molecular, and therapeutic aspects. Adv Cancer Res 88: 1-29.
20. Mossberg AK, Wullt B, Gustafsson L, Mansson W, Ljunggren E, et al. (2007) Bladder cancers respond to intravesical instillation of HAMLET (human alpha-lactalbumin made lethal to tumor cells). Int J Cancer 121: 1352-1359.
21. Fischer W, Gustafsson L, Mossberg AK, Gronli J, Mork S, et al. (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: 2105-2112.
22. Karpman D, Hakansson A, Perez MT, Isaksson C, Carlemalm E, et al. (1998) Apoptosis of renal cortical cells in the hemolytic-uremic syndrome: in vivo and in vitro studies. Infect Immun 66: 636-644.
23. Duringer C, Hamiche A, Gustafsson L, Kimura H, Svanborg C, (2003) HAMLET interacts with histones and chromatin in tumor cell nuclei. J Biol Chem 278: 42131-42135.
24. Aits S, Gustafsson L, Hallgren O, Brest P, Gustafsson M, et al. (2009) HAMLET (human alpha-lactalbumin made lethal to tumor cells) triggers autophagic tumor cell death. Int J Cancer 124: 1008-1019.
25. Thorne RF, Marshall JF, Shafren DR, Gibson PG, Hart IR, et al. (2000) The integrins alpha3beta1 and alpha6beta1 physically and functionally associate with CD36 in human melanoma cells. Requirement for the extracellular domain OF CD36. J Biol Chem 275: 35264-35275.
26. Liu J, Taylor DW, Taylor KA, (2004) A 3-D reconstruction of smooth muscle alpha-actinin by CryoEm reveals two different conformations at the actin-binding region. J Mol Biol 338: 115-125.
27. Koradi R, Billeter M, Wuthrich K, (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14: 51-55, 29-32.
28. Landegren U, (1984) Measurement of cell numbers by means of the endogenous enzyme hexosaminidase. Applications to detection of lymphokines and cell surface antigens. J Immunol Methods 67: 379-388.
29. Cuche E, Bevilacqua F, Depeursinge C, (1999) Digital holography for quantitative phase-contrast imaging. Opt Lett 24: 291-293.
30. Gustafsson M, Sebesta M, Bengtsson B, Pettersson SG, Egelberg P, et al. (2004) High-resolution digital transmission microscopy-a Fourier holography approach. Optics and Lasers in Engineering 41: 553-563.
31. Schnars U, Jüptner W, (2005) Digital holography: digital hologram recording, numerical reconstruction, and related techniques. ix, 164 Berlin; Heidelberg; New York Springer.
32. Dubois F, Yourassowsky C, Monnom O, Legros JC, Debeir O, et al. (2006) Digital holographic microscopy for the three-dimensional dynamic analysis of in vitro cancer cell migration. J Biomed Opt 11: 054032.
33. Sebesta M, Gustafsson M, (2005) Object characterization with refractometric digital Fourier holography. Opt Lett 30: 471-473.
34. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, et al. (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327-1333.
35. Baron MD, Davison MD, Jones P, Critchley DR, (1987) The structure and function of alpha-actinin. Biochem Soc Trans 15: 796-798.
36. Endo T, Masaki T, (1982) Molecular properties and functions in vitro of chicken smooth-muscle alpha-actinin in comparison with those of striated-muscle alpha-actinins. J Biochem 92: 1457-1468.
37. Ren J, Stuart DI, Acharya KR, (1993) Alpha-lactalbumin possesses a distinct zinc binding site. J Biol Chem 268: 19292-19298.
38. Bouchard V, Demers MJ, Thibodeau S, Laquerre V, Fujita N, et al. (2007) Fak/Src signaling in human intestinal epithelial cell survival and anoikis: differentiation state-specific uncoupling with the PI3-K/Akt-1 and MEK/Erk pathways. J Cell Physiol 212: 717-728.
39. Schlaepfer DD, Hauck CR, Sieg DJ, (1999) Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71: 435-478.
40. Fu L, Qin YR, Xie D, Chow HY, Ngai SM, et al. (2007) Identification of alpha-actinin 4 and 67 kDa laminin receptor as stage-specific markers in esophageal cancer via proteomic approaches. Cancer 110: 2672-2681.
41. Kikuchi S, Honda K, Tsuda H, Hiraoka N, Imoto I, et al. (2008) Expression and gene amplification of actinin-4 in invasive ductal carcinoma of the pancreas. Clin Cancer Res 14: 5348-5356.
42. Yamamoto S, Tsuda H, Honda K, Onozato K, Takano M, et al. (2009) Actinin-4 gene amplification in ovarian cancer: a candidate oncogene associated with poor patient prognosis and tumor chemoresistance. Mod Pathol 22: 499-507.
43. Hara T, Honda K, Shitashige M, Ono M, Matsuyama H, et al. (2007) Mass spectrometry analysis of the native protein complex containing actinin-4 in prostate cancer cells. Mol Cell Proteomics 6: 479-491.
44. Menez J, Le Maux Chansac B, Dorothee G, Vergnon I, Jalil A, et al. (2004) Mutant alpha-actinin-4 promotes tumorigenicity and regulates cell motility of a human lung carcinoma. Oncogene 23: 2630-2639.
45. Nikolopoulos SN, Spengler BA, Kisselbach K, Evans AE, Biedler JL, et al. (2000) The human non-muscle alpha-actinin protein encoded by the ACTN4 gene suppresses tumorigenicity of human neuroblastoma cells. Oncogene 19: 380-386.
46. Kaplan JM, Kim SH, North KN, Rennke H, Correia LA, et al. (2000) Mutations in ACTN4, encoding alpha-actinin-4, cause familial focal segmental glomerulosclerosis. Nat Genet 24: 251-256.
47. Kos CH, Le TC, Sinha S, Henderson JM, Kim SH, et al. (2003) Mice deficient in alpha-actinin-4 have severe glomerular disease. J Clin Invest 111: 1683-1690.
48. Craig DH, Downey C, Basson MD, (2008) SiRNA-mediated reduction of alpha-actinin-1 inhibits pressure-induced murine tumor cell wound implantation and enhances tumor-free survival. Neoplasia 10: 217-222.
49. Chiarugi P, Giannoni E, (2008) Anoikis: a necessary death program for anchorage-dependent cells. Biochem Pharmacol 76: 1352-1364.
50. 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.
51. Kohler C, Hakansson A, Svanborg C, Orrenius S, Zhivotovsky B, (1999) Protease activation in apoptosis induced by MAL. Exp Cell Res 249: 260-268.
52. Monteiro J, Fodde R, Cancer stemness and metastasis: therapeutic consequences and perspectives. Eur J Cancer 46: 1198-1203.
53. Thiery JP, (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454.
54. Di Vizio D, Kim J, Hager MH, Morello M, Yang W, et al. (2009) Oncosome formation in prostate cancer: association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res 69: 5601-5609.
55. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME, (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270: 1326-1331.
56. Zaoui K, Honore S, Isnardon D, Braguer D, Badache A, (2008) Memo-RhoA-mDia1 signaling controls microtubules, the actin network, and adhesion site formation in migrating cells. J Cell Biol 183: 401-408.