Targeting of a germ cell-specific type 1 hexokinase lacking a porin- binding domain to the mitochondria as well as to the head and fibrous sheath of murine spermatozoa

Molecular Biology of the Cell

Volumn 9, Issue 2, 1998, Pages 263-276

  Travis, Alexander J ^a   Foster, James A ^a   Rosenbaum, Nancy A ^a   Visconti, Pablo E ^a   Gerton, George L ^a   Kopf, Gregory S ^a   Moss, Stuart B ^a,b  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEXOKINASE; MEMBRANE PROTEIN; PORIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GERM CELL; IMMUNOELECTRON MICROSCOPY; MALE; MITOCHONDRION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON TAIL;

ANIMALIA; MURINAE;

EID: 0031930066     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.2.263     Document Type: Article

References (50)

1. Adams, V., Griffin, L.D., Gelb, B.D., and McCabe, E.R.B. (1991). Protein kinase activity of rat brain hexokinase. Biochem. Biophys. Res. Commun. 177, 1101-1106.
2. Adams, V., Schieber, A., and McCabe, E.R.B. (1994). Hexokinase autophosphorylation: identification of a new dual specificity protein kinase. Biochem. Med. Metab. Biol. 53, 80-86.
3. Arnold, H., and Pette, D. (1968). Binding of glycolytic enzymes to structural proteins of the muscle. Eur. J. Biochem. 6, 163-171.
4. Arora, K.K., Fanciulli, M., and Pederson, P.L. (1990). Glucose phosphorylation in tumor cells: cloning, sequencing and overexpression in active form of a full-length cDNA encoding a mitochondrial bindable form of hexokinase. J. Biol. Chem. 265, 6481-6488.
5. Arora, K.K., and Pedersen, P.L. (1988). Functional significance of mitochondrial bound hexokinase in tumor cell metabolism: evidence for preferential phosphorylation of glucose by intramitochondrially generated ATP. J. Biol. Chem. 263, 17422-17428.
6. Arora, K.K., and Pederson, P.L. (1993). Glucose utilization by tumor cells: the enzyme hexokinase autophosphorylates both its N- and C-terminal halves. Arch. Biochem. Biophys. 304, 515-518.
7. Bellvé, A.R., Millette, C.F., Bhatnagar, Y.M., and O'Brien, D. (1977). Dissociation of the mouse testis and characterization of isolated spermatogenic cells. J. Histochem. Cytochem. 25, 480-494.
8. Benau, D.A., McGuire, E.J., and Storey, B.T. (1990). Further characterization of the mouse sperm surface zona-binding site with galactosyltransferase activity. Mol. Reprod. Dev. 25, 393-399.
9. Benau, D.A., and Storey, B.T. (1988). Relationship between two types of mouse sperm surface sites that mediate binding of sperm to the zona pellucida. Biol. Reprod. 39, 235-244.
10. Bleil, J.D., and Wassarman, P.M. (1980). Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell 20, 873-882.
11. Bleil, J.D., and Wassarman, P.M. (1983). Sperm-egg interactions in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev. Biol. 95, 317-324.
12. Bordier, C. (1981). Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256, 1604-1607.
13. Capel, B., Swain, A., Nicolis, S., Hacker, A., Walter, M., Koopman, P., Goodfellow, P., and Lovell-Badge, R. (1993). Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 73, 1019-1030.
14. Carrera, A., Gerton, G.L., and Moss, S.B. (1994). The major fibrous sheath polypeptide of mouse sperm: structural and functional similarities to the A-kinase anchoring proteins. Dev. Biol. 165, 272-284.
15. Carrera, A., Moos, J., Ning, X.P., Gerton, G.L., Tesarik, J., Kopf, G.S., and Moss, S.B. (1996). Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin-dependent mechanism: identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation. Dev. Biol. 180, 284-296.
16. Cataldo, L., Baig, K., Oko, R., Mastrangelo, M., and Kleene, K.C. (1996). Developmental expression, intracellular localization, and selenium content of the cysteine-rich protein associated with the mitochondrial capsules of mouse sperm. Mol. Reprod. Dev. 45, 320-331.
17. Cooper, D.M., and Barondes, S.H. (1990). Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J. Cell Biol. 110, 1681-1691.
18. Ey, P.L., Prowse, S.J., and Jenkin, C.R. (1978). Isolation of pure IgG1, IgG2a and IgG2b immunoglobulins from mouse serum using protein A-Sepharose. Immunochemistry 15, 429-436.
19. Felgner, P.L., and Wilson, J.E. (1977). Effect of neutral salts on the interaction of rat brain hexokinase with the outer mitochondrial membrane. Arch. Biochem. Biophys. 182, 282-294.
20. Fujiki, Y., Hubbard, A.L., Fowler, S., and Lazarow, P.B. (1982). Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93, 97-102.
21. Garbers, D.L., Wakabayashi, T., and Reed, P.W. (1970). Enzyme profile of the cytoplasmic droplet from bovine epididymal spermatozoa. Biol. Reprod. 3, 327-337.
22. Gelb, B., Adams, V., Jones, S.N., Griffin, L.D., MacGregor, G.R., and McCabe, E.R.B. (1992). Targeting of hexokinase 1 to liver and hepatoma mitochondria. Proc. Natl. Acad. Sci. USA 89, 202-206.
23. Harrison, R.A.P., and White, I.G. (1972). Glycolytic enzymes in the spermatozoa and cytoplasmic droplets of bull, boar and ram, and their leakage after shock. J. Reprod. Fertil. 30, 105-115.
24. Hoppe, P.C. (1976). Glucose requirement for mouse sperm capacitation in vitro. Biol. Reprod. 15, 39-45.
25. Kalab, P., Visconti, P., Leclerc, P., and Kopf, G.S. (1994). p95, the major phosphotyrosine-containing protein in mouse spermatozoa, is a hexokinase with unique properties. J. Biol. Chem. 269, 3810-3817.
26. Katzen, H.M. (1967). The multiple forms of mammalian hexokinase and their significance to the action of insulin. Adv. Enzyme Regul. 5, 335-356.
27. Kew, D., Jin, D.F., Kim, F., Laddis, T., and Kilpatrick, D.L. (1989). Translational status of proenkephalin mRNA in the rat reproductive system. Mol. Endocrinol. 3, 1191-1196.
28. Kleene, K.C. (1996). Patterns of translational regulation in the mammalian testis. Mol. Reprod. Dev. 43, 268-281.
29. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
30. Leyton, L., LeGuen, P., Bunch, D., and Saling, P. (1992). Regulation of mouse gamete interaction by a sperm tyrosine kinase. Proc. Natl. Acad. Sci. USA 89, 11692-11695.
31. Leyton, L., and Saling, P. (1989). 95 kd sperm proteins bind ZP3 and serve as tyrosine kinase substrates in response to zona binding. Cell 57, 1123-1130.
32. Mori, C., Nakamura, N., Welch, J.E., Shiota, K., and Eddy, E.M. (1996). Testis-specific expression of mRNAs for a unique human type 1 hexokinase lacking the porin-binding domain. Mol. Reprod. Dev. 44, 14-22.
33. Mori, C., Welch, J.E., Fulcher, K.D., O'Brien, D.A., and Eddy, E.M. (1993). Unique hexokinase messenger ribonucleic acids lacking the porin-binding domain are develop mentally expressed in mouse spermatogenic cells. Biol. Reprod. 49, 191-203.
34. Naz, R.K., Morte, C., Ahmad, K., and Martinez, P. (1996). Hexokinase present in human sperm is not tyrosine phosphorylated but its antibodies affect fertilizing capacity. J. Androl. 17, 143-150.
35. O'Farrell, P.H. (1975). High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007-4021.
36. Olds-Clarke, P., Pilder, S.H., Visconti, P.E., Moss, S.B., Orth, J.M., and Kopf, G.S. (1996). Sperm from mice carrying two t haplotypes do not possess a tyrosine phosphorylated form of hexokinase. Mol. Reprod. Dev. 43, 94-104.
37. Pedley, K.C., Jones, G.E., Magnani, M., Rist, R.J., and Naftalin, R.J. (1993). Direct observation of hexokinase translocation in stimulated macrophages. Biochem. J. 291, 515-522.
38. Polakis, P.G., and Wilson, J.E. (1985). An intact hydrophobic N-terminal sequence is critical for binding of rat brain hexokinase to mitochondria. Arch. Biochem. Biophys. 236, 328-337.
39. Rapoport, T.A. (1992). Transport of proteins across the endoplasmic reticulum membrane. Science 258, 931-936.
40. Romrell, L.J., Bellvé, A.R., and Fawcett, D.W. (1976). Separation of mouse spermatogenic cells by sedimentation velocity. Dev. Biol. 49, 119-131.
41. Sampson, M.J., Lovell, R.S., and Craigen, W.J. (1997). The murine voltage-dependent anion channel gene family: conserved structure and function. J. Biol. Chem. 272, 18966-18973.
42. Schaffner, W., and Weissmann, C. (1973). A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal. Biochem. 56, 502-514.
43. Shur, B.D., and Hall, N.G. (1982). A role for mouse sperm surface galactosyltransferase in sperm binding to the egg zona pellucida. J. Cell Biol. 95, 574-579.
44. Smith, A.D., and Wilson, J.E. (1991). Disposition of mitochondrially bound hexokinase at the membrane surface, deduced from reactivity with monoclonal antibodies recognizing epitopes of defined location. Arch. Biochem. Biophys. 287, 359-366.
45. Storey, B.T. and Kayne, F.J. (1975). Energy metabolism of spermatozoa. V. The Embden-Myerhof pathway of glycolysis: activities of pathway enzymes in hypotonically treated rabbit epididymal spermatozoa. Fertil. Steril. 26, 1257-1265.
46. Tash, J.S. (1989). Protein phosphorylation: the second messenger signal transducer of flagellar motility. Cell Motil. Cytoskeleton 14, 332-339.
47. Urner, F., and Sakkas, D. (1996). Glucose participates in spermoocyte fusion in the mouse. Biol. Reprod. 55, 917-922.
48. Visconti, P.E., Olds-Clarke, P., Moss, S.B., Kalab, P., Travis, A.J., de las Heras, M., and Kopf, G.S. (1996). Properties and localization of a tyrosine phosphorylated form of hexokinase in mouse sperm. Mol. Reprod. Dev. 43, 82-93.
49. Westhoff, D., and Kamp, G. (1997). Glyceraldehyde 3-phosphate dehydrogenase is bound to the fibrous sheath of mammalian spermatozoa. J. Cell Sci. 110, 1821-1829.
50. Wilson, J.E. (1995). Hexokinases. Rev. Physiol. Biochem. Pharmacol. 126, 65-198.