LDHC: The ultimate testis-specific gene

Journal of Andrology

Volumn 31, Issue 1, 2010, Pages 86-94

  Goldberg, Erwin ^a   Eddy, Edward M ^b   Duan, Chongwen ^a   Odet, Fanny ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Glycolysis; Lactate dehydrogenase C; Male fertility; Sperm

Indexed keywords

LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE ISOENZYME 4; UNCLASSIFIED DRUG;

CONFERENCE PAPER; ENZYME REGULATION; ENZYME SPECIFICITY; FERTILIZATION; GEL ELECTROPHORESIS; GENE FUNCTION; HUMAN; IMMUNOHISTOCHEMISTRY; MALE FERTILITY; MEIOSIS; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON TAIL; TESTIS; TISSUE DISTRIBUTION;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; ISOENZYMES; L-LACTATE DEHYDROGENASE; MALE; SPERMATOZOA; TESTIS;

EID: 77749246456     PISSN: 01963635     EISSN: None     Source Type: Journal    
DOI: 10.2164/jandrol.109.008367     Document Type: Conference Paper

References (83)

1. Alcivar AA, Trasler JM, Hake LE, Salehi-Ashtiani K, Goldberg E, Hecht NB. DNA methylation and expression of the genes coding for lactate dehydrogenases A and C during rodent spermatogenesis. Biol Reprod. 1991;44:527-535.
2. Allen JM. Multiple forms of lactic dehydrogenase in tissues of the mouse: their specificity, cellular localization, and response to altered physiological conditions. Ann N Y Acad Sci. 1961;94:937-951.
3. Alvarez JG, Storey BT. Assessment of cell damage caused by spontaneous lipid peroxidation in rabbit spermatozoa. Biol Reprod. 1984;30:323-331.
4. Beyler SA, Wheat TE, Goldberg E. Binding of antibodies against antigenic domains of murine lactate dehydrogenase-C4 to human and mouse spermatozoa. Biol Reprod. 1985;32:1201-1210.
5. Blanco A, Burgos C, Gerez de Burgos NM, Montamat EE. Properties of the testicular lactate dehydrogenase isoenzyme. Biochem J. 1976;153:165-172.
6. Blanco A, Zinkham WH. Lactate dehydrogenases in human testes. Science. 1963;139:601-602.
7. Boer PH, Adra CN, Lau YF, McBurney MW. The testis-specific phosphoglycerate kinase gene pgk-2 is a recruited retroposon. Mol Cell Biol. 1987;7:3107-3112.
8. Bone W, Jones NG, Kamp G, Yeung CH, Cooper TG. Effect of ornidazole on fertility of male rats: inhibition of a glycolysis-related motility pattern and zona binding required for fertilization in vitro. J Reprod Fertil. 2000;118:127-135.
9. Bonny C, Goldberg E. The CpG-rich promoter of human LDH-C is differentially methylated in expressing and nonexpressing tissues. Dev Genet. 1995;16:210-217.
10. Boussouar F, Benahmed M. Lactate and energy metabolism in male germ cells. Trends Endocrinol Metab. 2004;15:345-350.
11. Burgos C, Maldonado C, Gerez de Burgos NM, Aoki A, Blanco A. Intracellular localization of the testicular and sperm-specific lactate dehydrogenase isozyme C4 in mice. Biol Reprod. 1995;53:84-92.
12. Cooker LA, Brooke CD, Kumari M, Hofmann MC, Millan JL, Goldberg E. Genomic structure and promoter activity of the human testis lactate dehydrogenase gene. Biol Reprod. 1993;48:1309-1319.
13. Coonrod S, Vitale A, Duan C, Bristol-Gould S, Herr J, Goldberg E. Testis-specific lactate dehydrogenase (LDH-C4; Ldh3) in murine oocytes and preimplantation embryos. J Androl. 2006;27:502-509.
14. Dewey MM, Conklin JL. Starch gel electrophoresis of lactic dehydrogenase from rat kidney. Proc Soc Exp Biol Med. 1960;105:492-494.
15. Duan C, Goldberg E. Inhibition of lactate dehydrogenase C4 (LDH-C4) blocks capacitation of mouse sperm in vitro. Cytogenet Genome Res. 2003;103:352-359.
16. Edwards Y, West L, Van Heyningen V, Cowell J, Goldberg E. Regional localization of the sperm-specific lactate dehydrogenase, LDHC, gene on human chromosome 11. Ann Hum Genet. 1989;53:215-219.
17. Erickson RP, Friend DS, Tennenbaum D. Localization of lactate dehydrogenase-X on the surfaces of mouse spermatozoa. Exp Cell Res. 1975a;91:1-5.
18. Erickson RP, Stites DP, Spielmann H. Effects on fertility of immunization against lactate dehydrogenase X in female mice. Contraception. 1975b;12:333-338.
19. Everse J, Kaplan NO. Lactate dehydrogenases: structure and function. Adv Enzymol Relat Areas Mol Biol. 1973;37:61-133.
20. Fujimoto H, Erickson RP, Tone S. Changes in polyadenylation of lactate dehydrogenase-X mRNA during spermatogenesis in mice. Mol Reprod Dev. 1988;1:27-34.
21. Gavella M, Cvitkovic P. Semen LDH-X deficiency and male infertility. Arch Androl. 1985;15:173-176.
22. Goldberg E. Lactic and malic dehydrogenases in human spermatozoa. Science. 1963;139:602-603.
23. Goldberg E. Lactate dehydrogenases and malate dehydrogenases in sperm: studied by Polyacrylamide gel electrophoresis. Ann N Y Acad Sci. 1964;121:560-570.
24. Goldberg E. Lactate dehydrogenases in spermatozoa: subunit interactions in vitro. Arch Biochem Biophys. 1965;109:134-141.
25. Goldberg E. Amino acid composition and properties of crystalline lactate dehydrogenase X from mouse testes. J Biol Chem. 1972;247:2044-2048.
26. Goldberg E. Infertility in female rabbits immunized with lactate dehydrogenase X. Science. 1973;181:458-159.
27. Goldberg E. Lactate dehydrogenase-X from mouse testes and spermatozoa. Methods Enzymol. 1975;41:318-323.
28. Goldberg E. Developmental expression of lactate dehydrogenase isozymes during spermatogenesis. Prog Clin Biol Res. 1990;344:49-52.
29. Goldberg E, Hawtrey C. The ontogeny of sperm specific lactate dehydrogenase in mice. J Exp Zool. 1967;164:309-316.
30. Goldberg E, VandeBerg JL, Mahony MC, Doncel GF. Immune response of male baboons to testis-specific LDH-C(4). Contraception. 2001;64:93-98.
31. Grootegoed JA, Jansen R, Van der Molen HJ. The role of glucose, pyruvate and lactate in ATP production by rat spermatocytes and spermatids. Biochim Biophys Acta. 1984;767:248-256.
32. Hintz M, Goldberg E. Immunohistochemical localization of LDH-x during spermatogenesis in mouse testes. Dev Biol. 1977;57:375-384.
33. Hogrefe HH, Griffith JP, Rossmann MG, Goldberg E. Characterization of the antigenic sites on the refined 3-A resolution structure of mouse testicular lactate dehydrogenase C4. J Biol Chem. 1987;262:13155-13162.
34. Jutte NH, Jansen R, Grootegoed JA, Rommerts FF, Clausen OP, van der Molen HJ. Regulation of survival of rat pachytene spermatocytes by lactate supply from Sertoli cells. J Reprod Fertit. 1982;65:431-438.
35. Krisfalusi M, Miki K, Magyar PL, O'Brien DA. Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol Reprod. 2006;75:270-278.
36. Kroft TL, Li S, Doglio L, Goldberg E. A transgenic analysis of mouse lactate dehydrogenase C promoter activity in the testis. J Androl. 2003;24:843-852.
37. Li S, Zhou W, Doglio L, Goldberg E. Transgenic mice demonstrate a testis-specific promoter for lactate dehydrogenase, LDHC. J Biol Chem. 1998;273:31191-31194.
38. Li SS. Lactate dehydrogenase isoenzymes A (muscle), B (heart) and C (testis) of mammals and the genes coding for these enzymes. Biochem Soc Trans. 1989;17:304-307.
39. Li SS, Feldmann RJ, Okabe M, Pan YC. Molecular features and immunological properties of lactate dehydrogenase C4 isozymes from mouse and rat testes. J Biol Chem. 1983a;258:7017-7028.
40. Li SS, Fitch WM, Pan YC, Sharief FS. Evolutionary relationships of vertebrate lactate dehydrogenase isozymes A4 (muscle), B4 (heart), and C4 (testis). J Biol Chem. 1983b;258:7029-7032.
41. Li SS, O'Brien DA, Hou EW, Versola J, Rockett DL, Eddy EM. Differential activity and synthesis of lactate dehydrogenase isozymes A (muscle), B (heart), and C (testis) in mouse spermatogenic cells. Biol Reprod. 1989;40:173-180.
42. Li YJ, Tsoi SC, Mannen H, Shoei-lung Li S. Phylogenetic analysis of vertebrate lactate dehydrogenase (LDH) multigene families. J Mol Evol. 2002;54:614-624.
43. Mahi-Brown CA, VandeVoort CA, McGuinness RP, Overstreet JW, O'Hern P, Goldberg E. Immunization of male but not female mice with the sperm-specific isozyme of lactate dehydrogenase (LDH-C4) impairs fertilization in vivo. Am J Reprod Immunol. 1990;24:1-8.
44. Mannen H, Tsoi SC, Krushkal JS, Li WH, Li SS. The cDNA cloning and molecular evolution of reptile and pigeon lactate dehydrogenase isozymes. Mol Biol Evol. 1997;14:1081-1087.
45. Markert CL, Amet TM, Goldberg E. Human testis-specific lactate dehydrogenase-C promoter drives overexpression of mouse lactate dehydrogenase-1 cDNA in testes of transgenic mice. J Exp Zool. 1998;282:171-178.
46. Markert CL, Appella E. Physicochemical nature of isozvmes. Ann N Y Acad Sci. 1961;94:678-690.
47. Markert CL, Shaklee JB, Whitt GS. Evolution of a gene: multiple genes for LDH isozymes provide a model of the evolution of gene structure, function and regulation. Science. 1975;189:102-114.
48. McCarrey JR, Thomas K. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature. 1987;326:501-505.
49. Miki K. Energy metabolism and sperm function. Soc Reprod Fertil Suppl. 2007;65:309-325.
50. Miki K, Qu W, Goulding EH, Willis WD, Bunch DO, Strader LF, Perreault SD, Eddy EM, O'Brien DA. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc Natl Acad Sci USA. 2004;101:16501-16506.
51. Millan JL, Driscoll CE, LeVan KM, Goldberg E. Epitopes of human testis-specific lactate dehydrogenase deduced from a cDNA sequence. Proc Natl Acad Sci USA. 1987;84:5311-5315.
52. Mita M, Hall PF. Metabolism of round spermatids from rats: lactate as the preferred substrate. Biol Reprod. 1982;26:445-455.
53. Montamat EE, Vermouth NT, Blanco A. Subcellular localization of branched-chain amino acid aminotransferase and lactate dehydrogenase C4 in rat and mouse spermatozoa. Biochem J. 1988;255:1053-1056.
54. Mukai C, Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod. 2004;71:540-547.
55. Musick WD, Rossmann MG. The structure of mouse testicular lactate dehydrogenase isoenzyme C4 at 2.9 A resolution. J Biol Chem. 1979;254:7611-7620.
56. Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM. A unique configuration of genome-wide DNA methylation patterns in the testis. Proc Natl Acad Sci U S A. 2007;104:228-233.
57. Odet F, Duan C, Willis WD, Goulding EH, Kung A, Eddy EM, Goldberg E. Expression of the gene for mouse lactate dehydrogenase C (Ldhc) is required for male fertility. Biol Reprod. 2008;79(1):26-34.
58. O'Flaherty CM, Beorlegui NB, Beconi MT. Lactate dehydrogenase-C4 is involved in heparin- and NADH-dependent bovine sperm capacitation. Andrologia. 2002;34(2):91-97.
59. O'Hern PA, Bambra CS, Isahakia M, Goldberg E. Reversible contraception in female baboons immunized with a synthetic epitope of sperm-specific lactate dehydrogenase. Biol Reprod. 1995;52:331-339.
60. Olsson PG, Tsujioka H, Narisawa S, Goldberg E, Millan JL. Abundance of repetitive sequence elements in the mouse testis-specific lactate dehydrogenase-C gene. J Androl. 2003;24:918-920.
61. Orlando C, Casano R, Caldini AL, Forti G, Barni T, Bonfanti L, Serio M. Measurement of seminal LDH-X and transferrin in normal and infertile men. J Androl. 1988;9:220-223.
62. Pan YC, Sharief FS, Okabe M, Huang S, Li SS. Amino acid sequence studies on lactate dehydrogenase C4 isozymes from mouse and rat testes. J Biol Chem. 1983;258:7005-7016.
63. Roller RJ, Kinloch RA, Hiraoka BY, Li SS, Wassarman PM. Gene expression during mammalian oogenesis and early embryogenesis: quantification of three messenger RNAs abundant in fully grown mouse oocytes. Development. 1989;106:251-261.
64. Salehi-Ashtiani K, Goldberg E. Posttranscriptional regulation of primate Ldhc mRNA by its AUUUA-like elements. Mol Endocrinol. 1995;9:1782-1790.
65. Shima JE, McLean DJ, McCarrey JR, Griswold MD. The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod. 2004;71:319-330.
66. Sleight SB, Miranda PV, Plaskett NW, Maier B, Lysiak J, Scrable H, Herr JC, Visconti PE. Isolation and proteomic analysis of mouse sperm detergent-resistant membrane fractions: evidence for dissociation of lipid rafts during capacitation. Biol Reprod. 2005;73: 721-729.
67. Smithies O. Zone electrophoresis in starch gels and its application to studies of serum proteins. Adv Protein Chem. 1959;14:65-113.
68. Takeno T, Li SS. Structure of the human lactate dehydrogenase B gene. Biochem J. 1989;257:921-924.
69. Tang H, Goldberg E. Homo sapiens lactate dehydrogenase c (Ldhc) gene expression in cancer cells is regulated by transcription factor Sp1, CREB, and CpG island methylation. J Androl. 2009;30:157-167.
70. Tang H, Kung A, Goldberg E. Regulation of murine lactate dehydrogenase C (Ldhc) gene expression. Biol Reprod. 2008;78: 455-461.
71. Thomas K, Del Mazo J, Eversole P, Bellve A, Hiraoka Y, Li SS, Simon M. Developmental regulation of expression of the lactate dehydrogenase (LDH) multigene family during mouse spermatogenesis. Development. 1990; 109:483-493.
72. Travis AJ, Jorgez CJ, Merdiushev T, Jones BH, Dess DM, Diaz-Cueto L, Storey BT, Kopf GS, Moss SB. Functional relationships between capacitation-dependent cell signaling and compartmentalized metabolic pathways in murine spermatozoa. J Biol Chem. 2001;276:7630-7636.
73. Urner F, Leppens-Luisier G, Sakkas D. Protein tyrosine phosphorylation in sperm during gamete interaction in the mouse: the influence of glucose. Biol Reprod. 2001;64:1350-1357.
74. Urner F, Sakkas D. Glucose participates in sperm-oocyte fusion in the mouse. Biol Reprod. 1996;55:917-922.
75. Urner F, Sakkas D. Protein phosphorylation in mammalian spermatozoa. Reproduction. 2003;125:17-26.
76. Welch JE, Brown PL, O'Brien DA, Magyar PL, Bunch DO, Mori C, Eddy EM. Human glyceraldehyde 3-phosphate dehydrogenase-2 gene is expressed specifically in spermatogenic cells. J Androl. 2000;21:328-338.
77. Welch JE, Schatte EC, O'Brien DA, Eddy EM. Expression of a glyceraldehyde 3-phosphate dehydrogenase gene specific to mouse spermatogenic cells. Biol Reprod. 1992;46:869-878.
78. Wheat TE, Goldberg E. Immunochemical dissection of the testes-specific isozyme lactate dehydrogenase C4. Ann N Y Acad Sci. 1984;438:156-170.
79. Williams AC, Ford WC. The role of glucose in supporting motility and capacitation in human spermatozoa. J Androl. 2001;22:680-695.
80. Zamudio NM, Chong S, O'Bryan MK. Epigenetic regulation in male germ cells. Reproduction. 2008;136:131-146.
81. Zhou W, Xu J, Goldberg E. A 60-bp core promoter sequence of murine lactate dehydrogenase C is sufficient to direct testis-specific transcription in vitro. Biol Reprod. 1994;51:425-432.
82. Zinkham WH, Blanco A, Clowry LJJr. An unusual isozyme of lactate dehydrogenase in mature testes: localization, ontogeny, and kinetic properties. Ann N Y Acad Sei. 1964;121:571-588.
83. Zinkham WH, Isensee H, Renwick JH. Linkage of lactate dehydrogenase B and C loci in pigeons. Science. 1969;164:185-187.