Glycomics and proteomics analyses of mouse uterine luminal fluid revealed a predominance of Lewis Y and X epitopes on specific protein carriers

Molecular and Cellular Proteomics

Volumn 8, Issue 2, 2009, Pages 325-342

  Kuo, Chu Wei ^a,b   Chen, Chin Mei ^b   Lee, Ying Chu ^b   Chus, Sin Tak ^b   Khoo, Kay Hooi ^b,c  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^c ACADEMIA SINICA   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GALACTOSE; GLYCAN; LACTOFERRIN; MANNOSE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE ANALYSIS; COMPARATIVE STUDY; EPIDIDYMIS; EPITOPE MAPPING; FEMALE; FUCOSYLATION; FUNCTIONAL PROTEOMICS; GLYCOBIOLOGY; HEAD; IMMUNITY; MALE; MALE GENITAL SYSTEM; MASS SPECTROMETRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN TRANSPORT; SEMINAL PLASMA; SIALYLATION; SPERMATOZOON MOTILITY; UTERUS;

ACUTE-PHASE PROTEINS; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD15; BODY FLUIDS; EPIDIDYMIS; EPITOPES; FEMALE; FUCOSE; GLYCOMICS; GLYCOPEPTIDES; GLYCOSYLATION; LEWIS BLOOD-GROUP SYSTEM; LIPOCALINS; MALE; MICE; MOLECULAR SEQUENCE DATA; NEURAMINIDASE; ONCOGENE PROTEINS; PROTEOME; PROTEOMICS; SEMINAL VESICLES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPERM MOTILITY; UTERUS;

EID: 61649111993     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M800320-MCP200     Document Type: Article

References (52)

1. Wasserman, P. M., Jovine, L., and Litscher, E. S. (2001) A profile of fertilization in mammals. Nat. Cell Biol. 3, E59-E64
2. Dell, A., Morris, H. R., Easton, R. L., Patankar, M., and Clark, G. F. (1999) The glycobiology of gametes and fertilization. Biochim. Biophys. Acta 1473, 196-205
3. Tulsiani, D. R., Yoshida-Komiya, H., and Araki, Y. (1997) Mammalian fertilization: a carbohydrate-mediated event. Biol. Reprod. 57, 487-494
4. Tulsiani, D. R. (2000) Structural analysis of the asparagine-linked glycan units of the ZP2 and ZP3 glycoproteins from mouse zone pellucida. Arch. Biochem. Biophys. 382, 275-283
5. Easton, R. L., Patankar, M. S., Lattanzio, F. A., Leaven, T. H., Morris, H. R., Clark, G. F., and Dell, A. (2000) Structural analysis of murine zone pellucida glycans. Evidence for the expression of core 2-type O-glycans and the Sd(a) antigen. J. Biol. Chem. 275, 7731-7742
6. Wasserman, P. M. (1988) Zone pellucida glycoproteins. Annu. Rev. Biochem. 57, 415-442
7. Schroter, S., Osterhoff, C., McArdle, W., and Ivell, R. (1999) The glycocalyx of the sperm surface. Hum. Reprod. Update 5, 302-313
8. Tulsiani, D. R., Orgebin-Crist, M. C., and Skudlarek, M. D. (1998) Role of luminal fluid glycosyltransferases and glycosidases in the modification of rat sperm plasma membrane glycoproteins during epididymal maturation. J. Reprod. Fertil. Suppl. 53, 85-97
9. Kurpisz, M., and Alexander, N. J. (1995) Carbohydrate moieties on sperm surface: physiological relevance. Fertil. Steril. 63, 158-165
10. McCauley, T. C., Kurth, B. E., Norton, E. J., Klotz, K. L., Westbrook, V. A., Rao, A. J., Herr, J. C., and Diekman, A. B. (2002) Analysis of a human sperm CD52 glycoform in primates: identification of an animal model for immunocontraceptive vaccine development. Biol. Reprod. 66, 1681-1688
11. Seppala, M., Taylor, R. N., Koistinen, H., Kolstinen, R., and Milgrom, E. (2002) Glycodelin: a major lipocalin protein of the reproductive axis with diverse actions in cell recognition and differentiation. Endocr. Rev. 23, 401-430
12. Yeung, W. S., Lee, K. F., Koistinen, R., Koistinen, H., Seppala, M., Ho, P. C., and Chiu, P. C. (2007) Glycodelin: a molecule with multi-functions on spermatozoa. Soc. Reprod. Fertil. Suppl. 63, 143-151
13. Akerstrom, B., Flower, D. R., and Selier, J. P. (2000) Lipocalins: unity in diversity. Biochim. Biophys. Acta 1482, 1-8
14. Morris, H. R., Dell, A., Easton, R. L., Panico, M., Koistinen, H., Koistinen, R., Oehninger, S., Patankar, M. S., Seppala, M., and Clark, G. F. (1996) Gender-specific glycosylation of human glycodelin affects its contraceptive activity. J. Biol. Chem. 271, 32159-32167
15. Keil, C., Husen, B., Giebel, J., Rune, G., and Walther, R. (1999) Glycodelin mRNA is expressed in the genital tract of male and female rats (Rattus norvegicus). J. Mol. Endocrinol. 23, 57-66
16. Chu, S. T., Huang, H. L., Chen, J. M., and Chen, Y. H. (1996) Demonstration of a glycoprotein derived from the 24p3 gene in mouse uterine luminal fluid. Biochem. J. 316, 545-550
17. Chu, S. T., Lee, Y. C., Nein, K. M., and Chen, Y. H. (2000) Expression, immunolocalization and sperm-association of a protein derived from 24p3 gene in mouse epididymis. Mol. Reprod. Dev. 57, 26-36
18. Kimber, S. J., and Spanswick, C. (2000) Blastocyst implantation: the adhesion cascade. Semin. Cell Dev. Biol. 11, 77-92
19. Ram, P. A., Cardullo, R. A., and Millette, C. F. (1989) Expression and topographical localization of cell surface fucosyltransferase activity during epididymal sperm maturation in the mouse. Gamete Res. 22, 321-332
20. Kimber, S. J., Stones, R. E., and Sidhu, S. S. (2001) Glycosylation changes during differentiation of the murine uterine epithelium. Biochem. Soc. Trans. 29, 156-162
21. Tulsiani, D. R., Skudlarek, M. D., Holland, M. K., and Orgebin-Crist, M. C. (1993) Glycosylation of rat sperm plasma membrane during epididymal maturation. Biol. Reprod. 48, 417-428
22. Domino, S. E., Zhang, L., Gillespie, P. J., Saunders, T. L., and Lowe, J. B. (2001) Deficiency of reproductive tract α(1,2)fucosylated glycans and normal fertility in mice with targeted deletions of the FUT1 or FUT2 α(1,2)fucosyltransferase locus. Mol. Cell. Biol. 21, 8336-8345
23. Smith, P. L., Myers, J. T., Rogers, C. E., Zhou, L, Petryniak, B., Becker, D. J., Homeister, J. W., and Lowe, J. B. (2002) Conditional control of selectin ligand expression and global fucosylation events in mice with a targeted mutation at the FX locus. J. Cell Biol. 158, 801-815
24. Hellbusch, C. C., Sperandio, M., Frommhold, D., Yakubenia, S., Wild, M. K., Popovici, D., Vestweber, D., Grone, H. J., von Figure, K., Lubke, T., and Korner, C. (2007) Golgi GDP-fucose transporter-deficient mice mimic congenital disorder of glycosylation IIc/leukocyte adhesion deficiency II. J. Biol. Chem. 282, 10762-10772
25. Lee, C. L., Hsiao, H. H., Lin, C. W., Wu, S. P., Huang, S. Y., Wu, C. Y., Wang, A. H., and Khoo, K. H. (2003) Strategic shotgun proteomics approach for efficient construction of an expression map of targeted protein families in hepatoma cell lines. Proteomics 3, 2472-2486
26. Ritchie, M. A., Gill, A. C., Deery, M. J., and Lilley, K. (2002) Precursor ion scanning for detection and structural characterization of heterogeneous glycopeptide mixtures. J. Am. Soc. Mass Spectrom. 13, 1065-1077
27. Dell, A., Reason, A. J., Khoo, K. H., Panico, M., McDowell, R. A., and Morris, H. R. (1994) Mass spectrometry of carbohydrate-containing biopolymers. Methods Enzymol. 230, 108-132
28. Guerardel, Y., Chang, L. Y., Maes, E., Huang, C. J., and Khoo, K. H. (2006) Glycomic survey mapping of zebrafish identifies unique sialylation pattern. Glycobiology 16, 244-257
29. Yu, S. Y., Wu, S. W., and Khoo, K. H. (2006) Distinctive characteristics of MALDI-Q/TOF and TOF/TOF tandem mass spectrometry for sequencing of permethylated complex type N-glycans. Glycoconj. J. 23, 355-369
30. Fan, Y. Y., Yu, S. Y., Ito, H., Akihiko, K., Sato, T., Lin, C. H., Yu, L. C., Narimatsu, H., and Khoo, K. H. (2008) Identification of further elongation and branching of dimeric type 1 chain on lactosyloeramides from colonic adenocarcinoma by tandem mass spectrometry sequencing analyses. J. Biol. Chem. 283, 16455-16468
31. Chu, S. T., Lin, H. J., and Chen, Y. H. (1997) Complex formation between a formyl peptide and 24p3 protein with a blocked N-terminus of pyroglutamate. J. Pept. Res. 49, 582-585
32. Lee, Y. C., Liao, C., Jr., Li, P. T., Tzeng, W. F., and Chu, S. T. (2003) Mouse lipocalin as an enhancer of spermatozoa motility. Mol. Biol. Rep. 30, 165-172
33. Ashline, D. J., Lapadula, A. J., Liu, Y. H., Lin, M., Grace, M., Pramanik, B., and Reinhold, V. N. (2007) Carbohydrate structural isomers analyzed by sequential mass spectrometry. Anal. Chem. 79, 3830-3842
34. Wu, A. M., Khoo, K. H., Yu, S. Y., Yang, Z., Kannagi, R., and Watkins, W. M. (2007) Glycomic mapping of pseudomucinous human ovarian cyst glycoproteins: identification of Lewis and sialyl Lewis glycotopes. Proteomics 7, 3699-3717
35. Wira, C. R., Fahey, J. V., Sentman, C. L., Pioli, P. A., and Shen, L. (2005) Innate and adaptive immunity in female genital tract: cellular responses and interactions. Immunol. Rev. 206, 306-335
36. Dasari, S., Pereira, L., Reddy, A. P., Michaels, J. E., Lu, X, Jacob, T., Thomas, A., Rodland, M., Roberts, C. T., Jr., Gravett, M. G., and Nagalla, S. R. (2007) Comprehensive proteomic analysis of human cervical-vaginal fluid. J. Proteome Res. 6, 1258-1268
37. Baveye, S., Elass, E., Fernig, D. G., Blanquart, C., Mazurier, J., and Legrand, D. (2000) Human lactoferrin interacts with soluble CD14 and inhibits expression of endothelial adhesion molecules, E-selectin and ICAM-1, induced by the CD14-lipopolysaccharide complex. Infect. Immun. 68, 6519-6525
38. Elass-Rochard, E., Legrand, D., Salmon, V., Roseanu, A., Trif, M., Tobias, P. S., Mazurier, J., and Spik, G. (1998) Lactoferrin inhibits the endotoxin interaction with CD14 by competition with the lipopolysaccharide-binding protein. Infect. Immun. 66, 486-491
39. Parmar, T., Sachdeva, G., Savardekar, L., Katkam, R. R., Nimbkar-Joshi, S., Gadkar-Sable, S., Salvi, V., Manjramkar, D. D., Meherji, P., and Puri, C. P. (2008) Protein repertoire of human uterine fluid during the mid-secretory phase of the menstrual cycle. Hum. Reprod. 23, 379-386
40. Luan, Y., and Xu, W. (2007) The structure and main functions of aminopeptidase N. Curr. Med. Chem. 14, 639-647
41. Katunuma, N., Matsunaga, Y., Himeno, K., and Hayashi, Y. (2003) Insights into the roles of cathepsins in antigen processing and presentation revealed by specific inhibitors. Biol. Chem. 384, 883-890
42. Ling, H., and Recklies, A. D. (2004) The chitinase 3-like protein human cartilage glycoprotein 39 inhibits cellular responses to the inflammatory cytokines interleukin-1 and tumour necrosis factor-α. Biochem. J. 380, 651-659
43. Lin, H. H., Li, W. W., Lee, Y. C., and Chu, S. T. (2007) Apoptosis induced by uterine 24p3 protein in endometrial carcinoma cell line. Toxicology 234, 203-215
44. Richardson, D. R. (2005) 24p3 and its receptor: dawn of a new iron age? Cell 123, 1175-1177
45. Liu, Q., and Nilsen-Hamilton, M. (1995) Identification of a new acute phase protein. J. Biol. Chem. 270, 22565-22570
46. Tong, Z., Wu, X., Ovcharenko, D., Zhu, J., Chen, C. S., and Kehrer, J. P. (2005) Neutrophil gelatinase-associated lipocalin as a survival factor. Biochem. J. 391, 441-448
47. Lee, Y. C., Elangovan, N., Tzeng, W. F., and Chu, S. T. (2005) Mouse uterine 24p3 protein as a suppressor of sperm acrosome reaction. Mol. Biol. Rep. 32, 237-245
48. Elangovan, N., Lee, Y. C., Tzeng, W. F., and Chu, S. T. (2004) Delivery of ferric ion to mouse spermatozoa is mediated by lipocalin internalization. Biochem. Biophys. Res. Commun. 319, 1096-1104
49. Kimber, S. J., and Lindenberg, S. (1990) Hormonal control of a carbohydrate epitope involved in implantation in mice. J. Reprod. Fertil. 89, 13-21
50. Chae, K., Lindzey, J., McLachlan, J. A., and Korach, K. S. (11998) Estrogen-dependent gene regulation by an oxidative metabolite of diethylstilbestrol, diethylstilbestrol-4′,4″-quinone. Steroids 63, 149-157
51. Jiang, X. Y., Smith, J. B., and Abraham, E. C. (1996) Identification of a MS-MS fragment diagnostic for methionine suffoxide. J. Mass Spectrom. 31, 1309-1310
52. Lagerwerf, F. M., van de Weert, M., Heerma, W., and Haverkamp, J. (1996) Identification of oxidized methionine in peptides. Rapid Commun. Mass Spectrom. 10, 1905-1910