Sialyl-glycoconjugates in cholesterol-rich microdomains of P388 cells are the triggers for apoptosis induced by Rana catesbeiana oocyte ribonuclease

Glycoconjugate Journal

Volumn 31, Issue 2, 2014, Pages 171-184

  Ogawa, Y ^a   Sugawara, S ^b   Tatsuta, T ^b   Hosono, M ^b   Nitta, K ^b   Fujii, Y ^a   Kobayashi, H ^a   Fujimura, T ^c   Taka, H ^c   Koide, Y ^d   Hasan, I ^d,e   Matsumoto, R ^d   Yasumitsu, H ^d   Kanaly, R A ^d   Kawsar, S M A ^d,f   Ozeki, Y ^d  

^a NAGASAKI INTERNATIONAL UNIVERSITY   (Japan)

^b TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^c JUNTENDO UNIVERSITY   (Japan)

^d YOKOHAMA CITY UNIVERSITY   (Japan)

^e UNIVERSITY OF RAJSHAHI   (Bangladesh)

^f UNIVERSITY OF CHITTAGONG   (Bangladesh)

Author keywords

Apoptosis; Caspase 3; Caspase 8; Cholesterol rich microdomain; Heat shock (cognate) protein 70; Lectin; Ribonuclease; Sialic acid

Indexed keywords

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; CHOLESTEROL; GLYCOCONJUGATES; HSC70 HEAT-SHOCK PROTEINS; HSP72 HEAT-SHOCK PROTEINS; LEUKEMIA P388; MEMBRANE MICRODOMAINS; MICE; N-ACETYLNEURAMINIC ACID; OOCYTES; RANA CATESBEIANA; RIBONUCLEASES;

EID: 84895102373     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-013-9513-7     Document Type: Article

References (43)

1. Nitta, K., Takayanagi, G., Kawauchi, H., Hakomori, S.: Isolation and characterization of Rana catesbeiana lectin and demonstration of the lectin-binding glycoprotein of rodent and human tumor cell membranes. Cancer Res. 47, 4877-4883 (1987)
2. Titani, K., Takio, K., Kuwada, M., Nitta, K., Sakakibara, F., Kawauchi, H., Takayanagi, G., Hakomori, S.: Amino acid sequence of sialic acid binding lectin from frog (Rana catesbeiana) eggs. Biochemistry 26, 2189-2194 (1987)
3. Nitta, R., Katayama, N., Okabe, Y., Iwama, M., Watanabe, H., Abe, Y., Okazaki, T., Ohgi, K., Irie, M.: Primary structure of a ribonuclease from bullfrog (Rana catesbeiana) liver. J. Biochem. 106, 729-735 (1989)
4. Nitta, K., Oyama, F., Oyama, R., Sekiguchi, K., Kawauchi, H., Takayanagi, Y., Hakomori, S., Titani, K.: Ribonuclease activity of sialic acid-binding lectin from Rana catesbeiana eggs. Glycobiology 3, 37-45 (1993)
5. Nitta, K., Ozaki, K., Tsukamoto, Y., Furusawa, S., Ohkubo, Y., Takimoto, H., Murata, R., Hosono, M., Hikichi, N., Sasaki, K., Kawauchi, H., Takayanagi, Y., Tsuiki, S., Hakomori, S.: Characterization of a Rana catesbeiana lectin-resistant mutant of leukemia P388 cells. Cancer Res. 54, 928-934 (1994)
6. Nitta, K., Ozaki, K., Tsukamoto, Y., Hosono, M., Ogawa-Konno, Y., Kawauchi, H., Takayanagi, Y., Tsuiki, S., Hakomori, S.: Catalytic lectin (leczyme) from bullfrog (Rana catesbeiana) eggs. Int. J. Oncol. 9, 19-23 (1996)
7. Nitta, K.: Leczyme. Methods Enzymol. 341, 368-374 (2001)
8. Wu, Y.N., Mikulski, S.M., Adelt, W., Rybak, S.M., Youle, R.J.: A cytotoxic ribonuclease. Study of the mechanism of onconase cytotoxicity. J. Biol. Chem. 268, 10668-10693 (1993)
9. Ardelt, W., Mikulski, S.M., Shogen, K.: Amino acid sequence of an anti-tumor protein from Rana pipiens oocytes and early embryos. Homology to pancreatic ribonucleases. J. Biol. Chem. 266, 245-251 (1991)
10. Liao, Y.D.: A pyrimidine-guanine sequence-specific ribonuclease from Rana catesbeiana (bullfrog) oocytes. Nucleic Acids Res. 20, 1371-1377 (1992)
11. Liao, Y.D., Wang, J.J.: Yolk granules are the major compartment for bullfrog (Rana catesbeiana) oocyte-specific ribonuclease. Eur. J. Biochem. 222, 215-220 (1994)
12. Liao, Y.D., Huang, H.C., Chan, H.J., Kuo, S.J.: Large-scale preparation of a ribonuclease from Rana catesbeiana (bullfrog) oocytes and characterization of its specific cytotoxic activity against tumor cells. Protein Expr. Purif. 7, 194-202 (1996)
13. Goparaju, C.M., Blasberg, J.D., Volinia, S., Palatini, J., Ivanov, S., Donington, J.S., Croce, C., Yang, H., Pass, H.I.: Onconase mediated NFKβ downregulation in malignant pleural mesothelioma. Oncogene 30, 2767-2777 (2011)
14. Nasu, M., Carbone, M., Gaudino, G., Ly, B.H., Bertino, P., Shimizu, D., Morris, P., Pass, H.I., Yang, H.: Ranpirnase interferes with NF-κB pathway pathway and MMP9 activity, inhibiting malignant mesothelioma cell invasiveness and xenograft growth. Genes Cancer 2, 576-584 (2011)
15. Hu, C.C., Tang, C.H., Wang, J.J.: Caspase activation in response to cytotoxic Rana catesbeiana ribonuclease in MCR-7 cells. FEBS Lett. 503, 65-68 (2001)
16. Tseng, H.H., Yu, Y.L., Chen, Y.L.S., Chen, J.H., Chou, C.L., Kou, T.Y., Wang, J.J., Lee, M.C., Huang, T.H., Chen, M.H.C., Yiang, G.T.: RC-RNase-induced cell death in estrogen receptor positive breast tumor through down-regulation of Bcl-2 and estrogen receptor. Oncol. Rep. 25, 849-853 (2011)
17. Chang, C.F., Chen, C., Chen, Y.C., Hom, K., Huang, R.F., Huang, T.H.: The solution structure of a cytotoxic ribonuclease from the oocytes of Rana catesbeiana (bullfrog). J. Mol. Biol. 283, 231-244 (1998)
18. Liu, J.H., Liao, Y.D., Sun, Y.J.: Crystallization and preliminary X-ray diffraction analysis of cytotoxic ribonucleases from bullfrog Rana catesbeiana. Acta Crystallogr. D Biol. Crystallogr. 57, 1697-1699 (2001)
19. Turcotte, R.F., Lavis, L.D., Raines, R.T.: Onconase cytotoxicity relies on the distribution of its positive charge. FEBS J. 276, 3846-3857 (2009)
20. Sundless, N.K., Raines, R.T.: Arginine residues are more effective than lysine residues in eliciting the cellular uptake of onconase. Biochemistry 50, 10293-10299 (2011)
21. Tennant, J.R.: Evaluation of the trypan blue technique for determination of cell viability. Transplantation 2, 685-694 (1964)
22. Vyas, H.K., Pal, R., Vishwakarma, R., Lohiya, N.K., Talwar, G.P.: Selective killing of leukemia and lymphoma cells ectopically expressing hCGβ by a conjugate of curcumin with an antibody against hCGβ subunit. Oncology 76, 101-111 (2009)
23. Pepper, C., Thomas, A., Tucker, H., Hoy, T., Bentley, P.: Flow cytometric assessment of three different methods for the measurement of in vivo apoptosis. Leuk. Res. 22, 439-444 (1998)
24. Sugawara, S., Hosono, M., Ogawa, Y., Takayanagi, M., Nitta, K.: Catfish egg lectin causes rapid activation of multidrug resistance 1 P-glycoprotein as a lipid translocase. Biol. Pharm. Bull. 28, 434-441 (2005)
25. Sugawara, S., Kawano, T., Omoto, T., Hosono, M., Tatsuta, T., Nitta, K.: Binding of Silurus asotus lectin to Gb3 on Raji cells causes disappearance of membrane-bound form of HSP70. Biochim. Biophys. Acta 1790, 101-109 (2009)
26. Gniadecki, R., Christoffersen, N., Wulf, H.C.: Cholesterol-rich plasma membrane domains (lipid rafts) in keratinocytes: importance in the baseline and UVA-induced generation of reactive oxygen species. J. Investig. Dermatol. 118, 582-588 (2001)
27. Hakomori, S., Handa, K.: Interaction of glycosphingolipids with signal transducers and membrane proteins in glycosphingolipid-enriched microdomains. Methods Enzymol. 363, 191-207 (2003)
28. Laemmli, U.K.: Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227, 680-685 (1970)
29. Matsudaira, P.: Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J. Biol. Chem. 262, 10035-10038 (1987)
30. Krajewski, S., Zapata, J.M., Reed, J.C.: Detection of multiple antigens on western blots. Anal. Biochem. 236, 221-228 (1996)
31. Hamaguchi, A., Suzuki, E., Murayama, K., Fujimura, T., Hikita, T., Iwabuchi, K., Handa, K., Withers, D.A., Casters, S.C., Fu, H., Hakomori, S.: Sphingosine-denependent protein kinase-1, directed to 14-3-3, is identified as the kinase domain of protein kinase Cd. J. Biol. Chem. 278, 41557-41565 (2003)
32. Perkins, D.N., Pappin, D.J.C., Creasy, D.M., Cottrell, J.S.: Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (1999)
33. Kamiya, Y., Oyama, F., Oyama, R., Sakakibara, F., Nitta, K., Kawauchi, H., Takayanagi, Y., Titani, K.: Amino acid sequence of a lectin from Japanese frog (Rana japonica) eggs. J. Biochem. 108, 139-143 (1990)
34. Morawski, M., Hartlage-Rubsamen, M., Jager, C., Waniek, A., Schilling, S., Schwab, C., McGeer, P.L., Arendt, T., Demuth, H.U., Rossner, S.: Distinct glutaminyl cyclase expression in Edinger-Westphal nucleus, locus coeruleus and nucleus basalis Meynert contributes to pGlu-Aβ pathology in Alzheimer's disease. Acta Neuropathol. 120, 195-207 (2010)
35. Chao, T.Y., Lavis, L.D., Raines, R.T.: Cellular uptake of ribonuclease A relies an anionic glycans. Biochemistry 49, 10666-10673 (2010)
36. Su, X., Sykes, J.B., Ao, L., Raeburn, C.D., Fullerton, D.A., Meng, X.: Extracellular heat shock cognate protein 70 induces cardiac functional tolerance to endotoxin: differential effect on TNF-α and ICAM-1 levels on heart tissue. Cytokine 51, 60-66 (2010)
37. Young, J.C., Barral, J.M., Hartl, F.U.: More than folding: localized functions of cytosolic chaperones. Trends Biochem. Sci. 28, 541-547 (2003)
38. Zou, N., Ao, L., Cleveland Jr., J.C., Yang, X., Su, X., Cai, G.Y., Banerjee, A., Fullerton, D.A., Meng, X.: Critical role of extracellular heat shock cognate protein 70 in the myocardial inflammatory response and cardiac dysfunction after global ischemia-reperfusion. Am. J. Physiol. Heart Circ. Physiol. 294, H2805-H2813 (2008)
39. Harada, Y., Sato, C., Kitajima, K.: Complex formation of 70 kDa heat shock protein with acidic glycolipids and phospholipids. Biochem. Biophys. Res. Commun. 353, 655-660 (2007)
40. Maehashi, E., Sato, C., Ohta, K., Harada, Y., Matsuda, T., Hirohashi, N., Lennarz, W.J., Kitajima, K.: Identification of the sea urchin 350-kDa sperm-binding protein as a new sialic acid-binding lectin that belongs to the heat shock protein 110 family: implication of its binding to gangliosides in sperm lipid rafts in fertilization. J. Biol. Chem. 278, 42050-42057 (2003)
41. Hatakeyama, S., Sugihara, K., Nakayama, J., Akama, T.O., Wong, S.M., Kawashima, H., Zhang, J., Smith, D.F., Ohyama, C., Fukuda, M., Fukuda, M.N.: Identification of mRNA splicing factors as the endothelial receptor for carbohydrate-dependent lung colonization of cancer cells. Proc. Natl. Acad. Sci. U. S. A. 106, 3095-3100 (2009)
42. Haudek, K.C., Patterson, R.J., Wang, J.L.: SP proteins and galectins: what's in a name? Glycobiology 20, 1199-1207 (2010)
43. Haudek, K.C., Spronk, K.J., Voss, P.G., Patterson, R.J., Wang, J.L., Arnoys, E.J.: Dynamics of galectin-3 in the nucleus and cytoplasm. Biochim. Biophys. Acta 1800, 181-189 (2010)