ApoA-I-binding Protein (AI-BP) and its Homologues hYjeF_N2 and hYjeF_N3 Comprise the YjeF_N Domain Protein Family in Humans with a Role in Spermiogenesis and Oogenesis

C. Rudolph; A. Sigruener; A. Hartmann; E. Orso; M. Bals-Pratsch; W. Gronwald; B. Seifert; H. R. Kalbitzer; I. Verdorfer; C. M. Luetjens; O. Ortmann; S. R. Bornstein; G. Schmitz

doi:10.1055/s-2007-977699

Hormone and Metabolic Research, Table of Contents

Horm Metab Res 2007; 39(5): 322-335
DOI: 10.1055/s-2007-977699

Original Basic

ApoA-I-binding Protein (AI-BP) and its Homologues hYjeF_N2 and hYjeF_N3 Comprise the YjeF_N Domain Protein Family in Humans with a Role in Spermiogenesis and Oogenesis

C. Rudolph¹ , A. Sigruener¹ , A. Hartmann² , E. Orso¹ , M. Bals-Pratsch³ , W. Gronwald⁴ , B. Seifert³ , H. R. Kalbitzer⁴ , I. Verdorfer⁵ , C. M. Luetjens⁶ , O. Ortmann⁷ , S. R. Bornstein⁸ , G. Schmitz¹

¹Institute of Clinical Chemistry and Laboratory Medicine, Regensburg University Medical Center, Regensburg, Germany
²Institute of Pathology, Regensburg University Medical Center, Regensburg, Germany
³Center for Gynecological Endocrinology, Reproductive Medicine and Human Genetics (CERMG), Regensburg, Germany
⁴Department of Biophysics and Physical Biochemistry, University of Regensburg, Regensburg, Germany
⁵Institute of Pathology, Medical University of Innsbruck, Innsbruck, Austria
⁶Institute of Reproductive Medicine, University of Muenster (WHO Collaboration Centre for Research in Male Reproduction), Muenster, Germany
⁷Department of Obstetrics and Gynecology, University of Regensburg, Caritas Hospital St. Josef, Regensburg, Germany
⁸Department of Medicine, University of Dresden, Dresden, Germany

Abstract

The screening for additional human YjeF_N domain containing proteins beside the apolipoprotein A-I interacting protein (AI-BP), identified two other genes designated hYjeF_N2-15q23 (formerly human homologue of yeast edc3) and hYjeF_N3-19p13.11 comprising the human YjeF_N family. AI-BP is ubiquitously expressed, with a predominance of these tissues where the homologues were found to be restricted including brain, mammary gland, testes and ovaries. Immunohistochemistry of human testes and ovaries showed an expression of hYjeF_N3-19p13.11 only in Leydig cells and theca cells, respectively, indicating a role in steroid hormone metabolism. Interestingly, the protein was also strongly expressed in Leydig cell tumors and in thecofibromas. The identification of hYjeF_N2-15q23 in theca cells and granulosa cells in ovaries, in human spermatids of meiotic division part II and the apical membrane of Sertoli cells in testes suggest similar functions in oogenesis and sperm maturation which is strengthened by the identification of the spermatogenesis regulator HMGA1 as a conserved transcription factor. However, in contrast to AI-BP, both homologous proteins are unable to bind apoA-I. These results relate the human YjeF_N domain containing protein family to cholesterol processing and steroid hormone metabolism in spermiogenesis and oogenesis, and AI-BP may link this function to the HDL pathway.

Key words

ABCA1 - ApoA-I - hYjeF_N1-1q21 - hedc3 - Leydig cells

Full Text

References

1 Gonzalez FA, Weisman GA, Erb L, Seye CI, Sun GY, Velazquez B, Hernandez-Perez M, Chorna NE. Mechanisms for inhibition of P2 receptors signaling in neural cells. Mol Neurobiol. 2005; 31 65-79
2 Lemmon MA. Pleckstrin homology domains: two halves make a hole?. Cell. 2005; 120 574-576
3 Li SS. Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem J. 2005; 390 641-653
4 Chance MR, Bresnick AR, Burley SK, Jiang JS, Lima CD, Sali A, Almo SC, Bonanno JB, Buglino JA, Boulton S, Chen H, Eswar N, He G, Huang R, Ilyin V, McMahan L, Pieper U, Ray S, Vidal M, Wang LK. Structural genomics: a pipeline for providing structures for the biologist Protein. Sci. 2002; 11 723-738
5 Ritter M, Buechler C, Boettcher A, Barlage S, Schmitz-Madry A, Orso E, Bared SM, Schmiedeknecht G, Baehr CH, Fricker G, Schmitz G. Cloning and characterization of a novel apolipoprotein A-I binding protein, AI-BP, secreted by cells of the kidney proximal tubules in response to HDL or ApoA-I. Genomics. 2002; 79 693-702
6 Albrecht M, Lengauer T. Novel Sm-like proteins with long C-terminal tails and associated methyltransferases. FEBS Lett. 2004; 569 18-26
7 Anantharaman V, Aravind L. Novel conserved domains in proteins with predicted roles in eukaryotic cell-cycle regulation, decapping and RNA stability BMC. Genomics. 2004; 5 45
8 Leipe DD, Koonin EV, Aravind L. Evolution and classification of P-loop kinases and related proteins. J Mol Biol. 2003; 333 781-815
9 Fenger-Gron M, Fillman C, Norrild B, Lykke-Andersen J. Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol Cell. 2005; 20 905-915
10 Chambenoit O, Hamon Y, Marguet D, Rigneault H, Rosseneu M, Chimini G. Specific docking of apolipoprotein A-I at the cell surface requires a functional ABCA1 transporter. J Biol Chem. 2001; 276 9955-9960
11 Martinez LO, Jacquet S, Esteve JP, Rolland C, Cabezon E, Champagne E, Pineau T, Georgeaud V, Walker JE, Terce F, Collet X, Perret B, Barbaras R. Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature. 2003; 421 75-79
12 Minnich A, Collet X, Roghani A, Cladaras C, Hamilton RL, Fielding CJ, Zannis VI. Site-directed mutagenesis and structure-function analysis of the human apolipoprotein A-I.Relation between lecithin-cholesterol acyltransferase activation and lipid binding. J Biol Chem. 1992; 267 16553-16560
13 Schmitz G, Robenek H, Lohmann U, Assmann G. Interaction of high density lipoproteins with cholesteryl ester-laden macrophages: biochemical and morphological characterization of cell surface receptor binding, endocytosis and resecretion of high density lipoproteins by macrophages. EMBO. J. 1985; 4 613-622
14 Takahashi Y, Smith JD. Cholesterol efflux to apolipoprotein AI involves endocytosis and resecretion in a calcium-dependent pathway. Proc Natl Acad Sci USA. 1999; 96 11358-11363
15 Schmitz G, Langmann T. Transcriptional regulatory networks in lipid metabolism control ABCA1 expression. Biochim Biophys Acta. 2005; 1735 1-19
16 Bodzioch M, Orso E, Klucken J, Langmann T, Bottcher A, Diederich W, Drobnik W, Barlage S, Buchler C, Porsch-Ozcurumez M, Kaminski WE, Hahmann HW, Oette K, Rothe G, Aslanidis C, Lackner KJ, Schmitz G. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet. 1999; 22 347-351
17 Moestrup SK, Nielsen LB. The role of the kidney in lipid metabolism. Current Opinion Lipidol. 2005; 16 301-306
18 Selva DM, Hirsch-Reinshagen V, Burgess B, Zhou S, Chan J, McIsaac S, Hayden MR, Hammond GL, Vogl AW, Wellington CL. The ATP-binding cassette transporter 1 mediates lipid efflux from Sertoli cells and influences male fertility. J Lipid Res. 2004; 45 1040-1050
19 Andersen OM, Yeung CH, Vorum H, Wellner M, Andreassen TK, Erdmann B, Mueller EC, Herz J, Otto A, Cooper TG, Willnow TE. Essential role of the apolipoprotein E receptor-2 in sperm development. J Biol Chem. 2003; 278 23989-23995
20 Huang LS, Voyiaziakis E, Chen HL, Rubin EM, Gordon JW. A novel functional role for apolipoprotein B in male infertility in heterozygous apolipoprotein B knockout mice. Proc Natl Acad Sci USA. 1996; 93 10903-10907
21 Wellington CL, Walker EK, Suarez A, Kwok A, Bissada N, Singaraja R, Yang YZ, Zhang LH, James E, Wilson JE, Francone O, McManus BM, Hayden MR. ABCA1 mRNA and protein distribution patterns predict multiple different roles and levels of regulation. Lab Invest. 2002; 82 273-283
22 Lawn RM, Wade DP, Couse TL, Wilcox JN. Localization of human ATP-binding cassette transporter 1 (ABC1) in normal and atherosclerotic tissues. Arterioscler Thromb Vasc Biol. 2001; 21 378-385
23 Pelletier RM, Byers SW. The blood-testis barrier and Sertoli cell junctions: structural considerations. Microsc Res Tech. 1992; 20 3-33
24 Mayerhofer A, Sinha Hikim AP, Bartke A, Russell LD. Changes in the testicular microvasculature during photoperiod-related seasonal transition from reproductive quiescence to reproductive activity in the adult golden hamster. Anat Rec. 1989; 224 495-507
25 Fofana M, Maboundou JC, Bocquet J, Le Goff D. Transfer of cholesterol between high density lipoproteins and cultured rat Sertoli cells. Biochem Cell Biol. 1996; 74 681-686
26 Andersen JM, Dietschy JM. Relative importance of high and low density lipoproteins in the regulation of cholesterol synthesis in the adrenal gland, ovary, and testis of the rat. J Biol Chem. 1978; 253 9024-9032
27 Dohle GR, Smit M, Weber RF. Androgens and male fertility. World J Urol. 2003; 21 341-345
28 Steinberger E, Root A, Ficher M, Smith KD. The role of androgens in the initiation of spermatogenesis in man. J Clin Endocrinol Metab. 1973; 37 746-751
29 McLachlan RI, Wreford NG, O'Donnell L, De Kretser DM, Robertson DM. The endocrine regulation of spermatogenesis: independent roles for testosterone and FSH. J Endocrinol. 1996; 148 1-9
30 Ryan KJ, Petro Z. Steroid biosynthesis by human ovarian granulosa and thecal cells. J Clin Endocrinol Metab. 1966; 26 46-52
31 Havelock JC, Rainey WE, Carr BR. Ovarian granulosa cell lines. Mol Cell Endocrinol. 2004; 228 67-78
32 Sasano H, Okamoto M, Mason JI, Simpson ER, Mendelson CR, Sasano N, Silverberg SG. Immunolocalization of aromatase, 17 alpha-hydroxylase and side-chain-cleavage cytochromes P-450 in the human ovary. J Reprod Fertil. 1989; 85 163-169
33 Bjersing L. On the morphology and endocrine function of granulosa cells in ovarian follicles and corpora lutea. Biochemical, histochemical, and ultrastructural studies on the porcine ovary with special reference to steroid hormone synthesis. Acta Endocrinol (Copenh). 1968; Suppl 23
34 Vihko P, Isomaa V, Ghosh D. Structure and function of 17beta-hydroxysteroid dehydrogenase type 1 and type 2. Mol Cell Endocrinol. 2001; 171 71-76
35 Devoto L, Kohen P, Vega M, Castro O, Gonzalez RR, Retamales I, Carvallo P, Christenson LK, Strauss JF. Control of human luteal steroidogenesis. Mol Cell Endocrinol. 2002; 186 137-141
36 Magoffin DA. Ovarian theca cell. Int J Biochem Cell Biol. 2005; 37 1344-1349
37 Jiang J-S, Gerchman SE, Manning NO, Eswaramoorthy S, Kumaran D, Kycia JH,, Lewis HA, Swaminathan S, Studier FW. Crystal Structure of Yeast Hypothetical Protein YNU0_YEAST. 2001; http://www.pdb.org. ;
38 Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ. Multiple sequence alignment with Clustal X. Trends Biochem Sci. 1998; 23 403-405
39 Moglich A, Weinfurtner D, Maurer T, Gronwald W, Kalbitzer HR. A restraint molecular dynamics and simulated annealing approach for protein homology modeling utilizing mean angles BMC. Bioinformatics. 2005; 6 91
40 Moglich A, Weinfurtner D, Gronwald W, Maurer T, Kalbitzer HR. PERMOL: restraint-based protein homology modeling using DYANA or CNS. Bioinformatics. 2005; 21 2110-2111
41 Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol. 1993; 234 779-815
42 Koradi R, Billeter M, Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph. 1996; 14 51-32
43 Palma PN, KrippahlL, Wampler JE, Moura JJ. BiGGER: a new (soft) docking algorithm for predicting protein interactions. Proteins. 2000; 39 372-384
44 Smith DF. Tetratricopeptide repeat cochaperones in steroid receptor complexes. Cell Stress Chaperones. 2004; 9 109-121
45 Duncan PI, Stojdl DF, Marius RM, Scheit KH, Bell JC. The Clk2 and Clk3 dual-specificity protein kinases regulate the intranuclear distribution of SR proteins and influence pre-mRNA splicing. Exp Cell Res. 1998; 241 300-308
46 Becker W, Kentrup H, Heukelbach J, Joost HG. cDNA cloning and characterization of rat Clk3, a LAMMER kinase predominately expressed in testis. Biochim Biophys Acta. 1996; 1312 63-67
47 Wang Y, Shao C, Shi CH, Zhang L, Yue HH, Wang PF, Yang B, Zhang YT, Liu F, Qin WJ, Wang H, Shao GX. Change of the cell cycle after flutamide treatment in prostate cancer cells and its molecular mechanism. Asian J Androl. 2005; 7 375-380
48 Menegay H, Moeslein F, Landreth G. The dual specificity protein kinase CLK3 is abundantly expressed in mature mouse spermatozoa. Exp Cell Res. 1999; 253 463-473
49 Tsuchiya Y, Nakajima M, Yokoi T. Cytochrome P450-mediated metabolism of estrogens and its regulation in human. Cancer Lett. 2005; 227 115-124
50 Jaiswal AK, Gonzalez FJ, Nebert DW. Human dioxin-inducible cytochrome P1-450: complementary DNA and amino acid sequence. Science. 1985; 228 80-83
51 Paolini M, Cantelli-Forti G, Perocco P, Pedulli GF, Abdel-Rahman SZ, Legator MS. Co-carcinogenic effect of beta-carotene. Nature. 1999; 398 760-761
52 Borhani DW, Rogers DP, Engler JA, Brouillette CG. Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation. Proc Natl Acad Sci USA. 1997; 94 12291-12296
53 Badis G, Saveanu C, Fromont-Racine M, Jacquier A. Targeted mRNA degradation by deadenylation-independent decapping. Mol Cell. 2004; 15 5-15
54 Kshirsagar M, Parker R. Identification of Edc3p as an enhancer of mRNA decapping in Saccharomyces cerevisiae. Genetics. 2004; 166 729-739
55 Travis AJ, Kopf GS. The role of cholesterol efflux in regulating the fertilization potential of mammalian spermatozoa. J Clin Invest. 2002; 110 731-736
56 Kierszenbaum AL. Mammalian spermatogenesis in vivo and in vitro: a partnership of spermatogenic and somatic cell lineages. Endocr Rev. 1994; 15 116-134
57 Liu J, Schiltz JF, Shah PC, Benson KF, Chada KK. Genomic structure and expression of the murine Hmgi(y) gene. Gene. 2000; 246 197-207
58 Liu J, Schiltz JF, Ashar HR, Chada KK. Hmga1 is required for normal sperm development. Mol Reprod Dev. 2003; 66 81-89
59 Jaffe J, Hochberg M, Riss J, Hasin T, Reich L, Laskov R. Cloning, sequencing and expression of two isoforms of the murine oct-1 transcription factor. Biochim Biophys Acta. 1995; 1261 201-209
60 Riss J, Laskov R. Expression of novel alternatively spliced isoforms of the oct-1 transcription factor. Biochim Biophys Acta. 1999; 1444 295-298
61 Scieglinska D, Vydra N, Krawczyk Z, Widlak W. Location of promoter elements necessary and sufficient to direct testis-specific expression of the Hst70/Hsp70.2 gene. Biochem J. 2004; 379 739-747
62 Fallone F, Villard PH, Seree E, Rimet O, Nguyen QB, Bourgarel-Rey V, Fouchier F, Barra Y, Durand A, Lacarelle B. Retinoids repress Ah receptor CYP1A1 induction pathway through the SMRT corepressor. Biochem Biophys Res Commun. 2004; 322 551-556
63 Chung SS, Wang X, Wolgemuth DJ. Male sterility in mice lacking retinoic acid receptor alpha involves specific abnormalities in spermiogenesis. Differentiation. 2005; 73 188-198
64 Augusto D, Leteurtre E, De La TA, Gosselin B, Leroy X. Calretinin: a valuable marker of normal and neoplastic Leydig cells of the testis. Appl Immunohistochem Mol Morphol. 2002; 10 159-162
65 Cheville JC, Sebo TJ, Lager DJ, Bostwick DG, Farrow GM. Leydig cell tumor of the testis: a clinicopathologic, DNA content, and MIB-1 comparison of nonmetastasizing and metastasizing tumors. Am J Surg Pathol. 1998; 22 1361-1367

Correspondence

Prof. Dr. G. Schmitz

Institute of Clinical Chemistry and Laboratory Medicine

Regensburg University Medical Center

Franz-Josef-Strauß-Allee 11

93053 Regensburg

Germany

Phone: +49/941/944 62 01

Fax: +49/941/944 62 02

Email: gerd.schmitz@klinik.uni-regensburg.de