Compartmentalization of a unique ADP/ATP carrier protein SFEC (Sperm Flagellar Energy Carrier, AAC4) with glycolytic enzymes in the fibrous sheath of the human sperm flagellar principal piece

Developmental Biology

Volumn 302, Issue 2, 2007, Pages 463-476

  Kim, Young Hwan ^a   Haidl, Gerhard ^b   Schaefer, Martina ^c   Egner, Ursula ^c   Mandal, Arabinda ^c   Herr, John C ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF BONN   (Germany)

^c BAYER PHARMA AG   (Germany)

Author keywords

ADP ATP carrier; Energy production; Energy translocation; Fibrous sheath; Glycolytic enzymes; Principal piece; Sperm flagellar energy carrier; Sperm glycolysis; Sperm motility

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLYCOLYTIC ENZYME; IDITOL DEHYDROGENASE; MULTIENZYME COMPLEX; NUCLEOTIDE BINDING PROTEIN; PYRUVATE KINASE;

ANIMAL EXPERIMENT; ARTICLE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; DRUG TARGETING; ENERGY CONSUMPTION; ENERGY YIELD; ENZYME LOCALIZATION; ENZYME SUBSTRATE; FLAGELLUM; GLYCOLYSIS; HUMAN; IMMUNOFLUORESCENCE; MALE; MASS SPECTROMETRY; MITOCHONDRIAL RESPIRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; PROTEOMICS; RESPIRATORY CHAIN; SEQUENCE HOMOLOGY; SPERMATOGENESIS; SPERMATOZOON MOTILITY; SPERMATOZOON TAIL; TENDON SHEATH;

EID: 33846818727     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.10.004     Document Type: Article

References (67)

1. Burant C.F., Takeda J., Brot-Laroche E., Bell G.I., and Davidson N.O. Fructose transporter in human spermatozoa and small intestine is GLUT5. J. Biol. Chem. 267 (1992) 14523-14526
2. Cao W., Gerton G.L., and Moss S.B. Proteomic profiling of accessory structures from the mouse sperm flagellum. Mol. Cell. Proteomics 5 (2006) 801-810
3. Casslen B., and Nilsson B. Human uterine fluid, examined in undiluted samples for osmolarity and the concentrations of inorganic ions, albumin, glucose, and urea. Am. J. Obstet. Gynecol. 150 (1984) 877-881
4. Chen Y., Cann M.J., Litvin T.N., Iourgenko V., Sinclair M.L., Levin L.R., and Buck J. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289 (2000) 625-628
5. Chung F.Z., Tsujibo H., Bhattacharyya U., and Sharief F.S. Genomic organization of human lactate dehydrogenase-A gene. Biochem. J. 231 (1985) 537-541
6. Cozens A.L., Runswick M.J., and Walker J.E. DNA sequences of two expressed nuclear genes for human mitochondrial ADP/ATP translocase. J. Mol. Biol. 206 (1989) 261-280
7. Dehal P., Predki P., Olsen A.S., Kobayashi A., Folta P., Lucas S., Land M., Terry A., Ecale Zhou C.L., Rash S., Zhang Q., Gordon L., Kim J., Elkin C., Pollard M.J., Richardson P., Rokhsar D., Uberbacher E., Hawkins T., Branscomb E., and Stubbs L. Human chromosome 19 and related regions in mouse: conservative and lineage-specific evolution. Science 293 (2001) 104-111
8. Dolce V., Scarcia P., Iacopetta D., and Palmieri F. A fourth ADP/ATP carrier isoform in man: identification, bacterial expression, functional characterization and tissue distribution. FEBS Lett. 579 (2005) 633-637
9. Duyckaerts C., Sluse-Goffart C.M., Fux J.P., Sluse F.E., and Liebecq C. Kinetic mechanism of the exchanges catalysed by the adenine-nucleotide carrier. Eur. J. Biochem. 106 (1980) 1-6
10. Edwards Y., West L., Van Heyningen V., Cowell J., and Goldberg E. Regional localization of the sperm-specific lactate dehydrogenase, LDHC, gene on human chromosome 11. Ann. Hum. Genet. 53 (1989) 215-219
11. Ellison J.W., Li X., Francke U., and Shapiro L.J. Rapid evolution of human pseudoautosomal genes and their mouse homologs. Mamm. Genome 7 (1996) 25-30
12. Ercolani L., Florence B., Denaro M., and Alexander M. Isolation and complete sequence of a functional human glyceraldehyde-3-phosphate dehydrogenase gene. J. Biol. Chem. 263 (1988) 15335-15341
13. Fawcett D.W. The mammalian spermatozoon. Dev. Biol. 44 (1975) 44394-44436
14. Frenkel G., Peterson R.N., and Freund M. Oxidative and glycolytic metabolism of semen components by washed guinea pig spermatozoa. Fertil. Steril. 26 (2002) 144-147
15. Fujita A., Nakamura K., Kato T., Watanabe N., Ishizaki T., Kimura K., Mizoguchi A., and Narumiya S. Ropporin, a sperm-specific binding protein of rhophilin, that is localized in the fibrous sheath of sperm flagella. J. Cell Sci. 113 (2000) 103-112
16. Fulcher K.D., Mori C., Welch J.E., O'Brien D.A., Klapper D.G., and Eddy E.M. Characterization of Fsc1 cDNA for a mouse sperm fibrous sheath component. Biol. Reprod. 52 (1995) 41-49
17. Geer L.Y., Domrachev M., Lipman D.J., and Bryant S.H. CDART: protein homology by domain architecture. Genome Res. (2002) 121619-121623
18. Gillis B.A., and Tamblyn T.M. Association of bovine sperm aldolase with sperm subcellular components. Biol. Reprod. 31 1 (1984) 25-35
19. Graham B.H., Waymire K.G., Cottrell B., Trounce I.A., MacGregor G.R., and Wallace D.C. A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nat. Genet. 16 (1997) 226-234
20. Haraguchi Y., Chung A.B., Torroni A., Stepien G., Shoffner J.M., Wasmuth J.J., Costigan D.A., Polak M., Altherr M.R., Winokur S.T., and Wallace D.C. Genetic mapping of human heart-skeletal muscle adenine nucleotide translocator and its relationship to the facioscapulohumeral muscular dystrophy locus. Genomics 16 (1993) 479-485
21. Hers H.G. The mechanism of the transformation of glucose in fructose in the seminal vesicles. Biochim. Biophys. Acta 22 (1956) 202-203
22. Iwata T., Popescu N.C., Zimonjic D.B., Karlsson C., Hoog J.O., Vaca G., Rodriguez I.R., and Carper D. Structural organization of the human sorbitol dehydrogenase gene (SORD). Genomics 26 (1995) 55-62
23. Izzo P., Costanzo P., Lupo A., Rippa E., Paolella G., and Salvatore F. Human aldolase A gene. Structural organization and tissue-specific expression by multiple promoters and alternate mRNA processing. Eur. J. Biochem. 174 (1988) 569-578
24. Kim Y.H., de Kretser D.M., Temple-Smith P.D., Hearn M.T., and McFarlane J.R. Isolation and characterization of human and rabbit sperm tail fibrous sheath. Mol. Hum. Reprod. 3 (2005) 307-313
25. Kim Y.H., Jha K.N., Mandal A., Vanage G., Farris E., Snow P.L., Klotz K., Naaby-Hansen S., Flickinger C.J., and Herr J.C. Translation and assembly of CABYR coding region B in fibrous sheath and restriction of calcium binding to coding region A. Dev. Biol. 286 (2005) 46-56
26. King T.E., and Mann T. Sorbitol dehydrogenase in spermatozoa. Nature 182 (1958) 868-869
27. Klingenberg M. Membrane protein oligomeric structure and transport function. Nature 290 (1981) 449-454
28. Kobayashi T., Kaneko T., Iuchi Y., Matsuki S., Takahashi M., Sasagawa I., Nakada T., and Fujii J. Localization and physiological implication of aldose reductase and sorbitol dehydrogenase in reproductive tracts and spermatozoa of male rats. J. Androl. 23 (2002) 674-683
29. Krisfalusi M., Miki K., Magyar P.L., and O'brien D.A. Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol. Reprod. 75 (2006) 270-278
30. Ku D.H., Kagan J., Chen S.T., Chang C.D., Baserga R., and Wurzel J. The human fibroblast adenine nucleotide translocator gene. Molecular cloning and sequence. J. Biol. Chem. 265 (1990) 16060-16063
31. Lasorsa F.M., Scarcia P., Erdmann R., Palmieri F., Rottensteiner H., and Palmieri L. The yeast peroxisomal adenine nucleotide transporter: characterization of two transport modes and involvement in DeltapH formation across peroxisomal membranes. Biochem. J. 381 (2004) 581-585
32. Leese H.J., Astley N.R., and Lambert D. Glucose and fructose utilization by rat spermatozoa within the uterine lumen. J. Reprod. Fertil. 61 (1981) 435-437
33. Levy S.E., Chen Y.S., Graham B.H., and Wallace D.C. Expression and sequence analysis of the mouse adenine nucleotide translocase 1 and 2 genes. Gene 254 (2000) 57-66
34. Lindemann C.B., Orlando A., and Kanous K.S. The flagellar beat of rat sperm is organized by the interaction of two functionally distinct populations of dynein bridges with a stable central axonemal partition. J. Cell Sci. 102 (1992) 249-260
35. Mandal A., Naaby-Hansen S., Wolkowicz M.J., Klotz K., Shetty J., Retief J.D., Coonrod S.A., Kinter M., Sherman N., Cesar F., Flickinger C.J., and Herr J.C. FSP95, a testis-specific 95-kilodalton fibrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa. Biol. Reprod. 61 (1999) 1184-1197
36. Maquat L.E., Chilcote R., and Ryan P.M. Human triosephosphate isomerase cDNA and protein structure. Studies of triosephosphate isomerase deficiency in man. J. Biol. Chem. 260 (1985) 3748-3753
37. Miki K., Qu W., Goulding E.H., Willis W.D., Bunch D.O., Strader L.F., Perreault S.D., Eddy E.M., and O'Brien D.A. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 16501-16506
38. Mitchell B.F., Pedersen L.B., Feely M., Rosenbaum J.L., and Mitchell D.R. ATP production in Chlamydomonas reinhardtii flagella by glycolytic enzymes. Mol. Biol. Cell 16 (2005) 4509-4518
39. Mohri H., Mohri T., and Ernster L. Isolation and enzymatic properties of the midpiece of bull spermatozoa. Exp. Cell Res. 38 (1965) 217-246
40. Mori C., Nakamura N., Welch J.E., Gotoh H., Goulding E.H., Fujioka M., and Eddy E.M. Mouse spermatogenic cell-specific type 1 hexokinase (mHk1-s) transcripts are expressed by alternative splicing from the mHk1 gene and the HK1-S protein is localized mainly in the sperm tail. Mol. Reprod. Dev. 49 (1998) 374-385
41. Mukai C., and Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol. Reprod. 71 (2004) 540-547
42. Murdoch R.N., and White I.G. Studies of the metabolism of human spermatozoa. J. Reprod. Fertil. 16 (1968) 351-361
43. Naaby-Hansen S., Mandal A., Wolkowicz M.J., Sen B., Westbrook V.A., Shetty J., Coonrod S.A., Klotz K.L., Kim Y.H., Bush L.A., Flickinger C.J., and Herr J.C. CABYR, a novel calcium-binding tyrosine phosphorylation-regulated fibrous sheath protein involved in capacitation. Dev. Biol. 242 (2002) 236-254
44. Nakamura K., Fujita A., Murata T., Watanabe G., Mori C., Fujita J., Watanabe N., Ishizaki T., Yoshida O., and Narumiya S. Rhophilin, a small GTPase Rho-binding protein, is abundantly expressed in the mouse testis and localized in the principal piece of the sperm tail. FEBS Lett. 445 (1999) 9-13
45. Nelson D.R., Felix C.M., and Swanson J.M. Highly conserved charge-pair networks in the mitochondrial carrier family. J. Mol. Biol. 277 (1998) 285-308
46. O'Shea T., and Wales R.G. Metabolism of sorbitol and fructose by ram spermatozoa. J. Reprod. Fertil. 10 (1965) 353-368
47. Palmieri L., Rottensteiner H., Girzalsky W., Scarcia P., Palmieri F., and Erdmann R. Identification and functional reconstitution of the yeast peroxisomal adenine nucleotide transporter. EMBO J. 20 (2001) 5049-5059
48. Palmieri L., Alberio S., Pisano I., Lodi T., Meznaric-Petrusa M., Zidar J., Santoro A., Scarcia P., Fontanesi F., Lamantea E., Ferrero I., and Zeviani M. Complete loss-of-function of the heart/muscle-specific adenine nucleotide translocator is associated with mitochondrial myopathy and cardiomyopathy. Hum. Mol. Genet. 14 (2005) 3079-3088
49. Pazour G.J., Agrin N., Leszyk J., and Witman G.B. Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170 (2005) 103-113
50. Pebay-Peyroula E., Dahout-Gonzalez C., Kahn R., Trezeguet V., Lauquin G.J., and Brandolin G. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426 (2003) 39-44
51. Schiebel K., Weiss B., Wohrle D., and Rappold G. A human pseudoautosomal gene, ADP/ATP translocase, escapes X-inactivation whereas a homologue on Xq is subject to X-inactivation. Nat. Genet. 3 (1993) 82-87
52. Slim R., Levilliers J., Ludecke H.J., Claussen U., Nguyen V.C., Gough N.M., Horsthemke B., and Petit C. A human pseudoautosomal gene encodes the ANT3 ADP/ATP translocase and escapes X-inactivation. Genomics 16 (1993) 26-33
53. Stepien G., Torroni A., Chung A.B., Hodge J.A., and Wallace D.C. Differential expression of adenine nucleotide translocator isoforms in mammalian tissues and during muscle cell differentiation. J. Biol. Chem. 267 (1992) 14592-14597
54. Storey B.T., and Kayne F.J. Energy metabolism of spermatozoa: V. The Embden-Myerhof pathway of glycolysis: activities of pathway enzymes in hypotonically treated rabbit epididymal spermatozoa. Fertil. Steril. 26 12 (1975) 1257-1265
55. Storey B.T., and Kayne F.J. Energy metabolism of spermatozoa: VII. Interactions between lactate, pyruvate and malate as oxidative substrates for rabbit sperm mitochondria. Biol. Rreprod. 18 4 (1978) 527-536
56. Sullivan D.T., MacIntyre R., Fuda N., Fiori J., Barrilla J., and Ramizel L. Analysis of glycolytic enzyme co-localization in Drosophila flight muscle. J. Exp. Biol. 206 (2003) 2031-2038
57. Travis A.J., Foster J.A., Rosenbaum N.A., Visconti P.E., Gerton G.L., Kopf G.S., and Moss S.B. 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. Mol. Biol. Cell 9 (1998) 263-276
58. Travis A.J., Jorgez C.J., Merdiushev T., Jones B.H., Dess D.M., Diaz-Cueto L., Storey B.T., Kopf G.S., and Moss S.B. Functional relationships between capacitation-dependent cell signaling and compartmentalized metabolic pathways in murine spermatozoa. J. Biol. Chem. 276 (2001) 7630-7636
59. Tsutsumi H., K.Tani H., and Fujii S. Expression of L- and M-type pyruvate kinase in human tissues. Genomics 2 (1988) 86-89
60. Turner R.M., Johnson L.R., Haig-Ladewig L., Gerton G.L., and Moss S.B. An X-linked gene encodes a major human sperm fibrous sheath protein, hAKAP82. Genomic organization, protein kinase A-RII binding, and distribution of the precursor in the sperm tail. J. Biol. Chem. 273 (1998) 32135-32141
61. Vijayaraghavan S., Liberty G.A., Mohan J., Winfrey V.P., Olson G.E., and Carr D.W. Isolation and molecular characterization of AKAP110, a novel, sperm-specific protein kinase A-anchoring protein. Mol. Endocrinol. 13 (1999) 705-717
62. Visconti P.E., and Kopf G.S. Regulation of protein phosphorylation during sperm capacitation. Biol. Reprod. 59 (1998) 1-6
63. Walker J.E., and Runswick M.J. The mitochondrial transport protein superfamily. J. Bioenerg Biomembr. 25 (1993) 435-446
64. Welch J.E., Schatte E.C., O'Brien D.A., and Eddy E.M. Expression of a glyceraldehyde 3-phosphate dehydrogenase gene specific to mouse spermatogenic cells. Biol. Reprod. 46 (1992) 869-878
65. Welch J.E., Brown P.L., O'Brien D.A., Magyar P.L., Bunch D.O., Mori C., and Eddy E.M. Human glyceraldehyde 3-phosphate dehydrogenase-2 gene is expressed specifically in spermatogenic cells. J. Androl. 21 (2000) 328-338
66. Westhoff D., and Kamp G. Glyceraldehyde 3-phosphate dehydrogenase is bound to the fibrous sheath of mammalian spermatozoa. J. Cell Sci. 110 (1997) 1821-1829
67. Wojtas K., Slepecky N., von Kalm L., and Sullivan D. Flight muscle function in Drosophila requires colocalization of glycolytic enzymes. Mol. Biol. Cell 8 (1997) 1665-1675