LGR4 regulates the postnatal development and integrity of male reproductive tracts in mice

Biology of Reproduction

Volumn 76, Issue 2, 2007, Pages 303-313

  Hoshii, Takayuki ^a   Takeo, Toru ^a   Nakagata, Naomi ^a   Takeya, Motohiro ^a   Araki, Kimi ^b   Yamamura, Ken Ichi ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b School of Medicine ^*

Author keywords

Developmental biology; Epididymis; Estradiol receptor; Male reproductive tract; Steroid hormone receptors

Indexed keywords

ESTROGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 4; LAMININ; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; ELECTRON MICROSCOPY; EPIDIDYMIS DISEASE; EPIDIDYMIS TAIL; FEMALE; GROWTH RETARDATION; MALE; MALE GENITAL SYSTEM; MALE INFERTILITY; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RETE TESTIS; SEMINIFEROUS TUBULE; SPERMATOZOON MOTILITY; TESTIS DEVELOPMENT; TESTIS DISEASE;

ANIMALS; ANIMALS, NEWBORN; CELL LINE; DOWN-REGULATION; EPIDIDYMIS; ESTROGEN RECEPTOR ALPHA; FEMALE; GENITALIA, MALE; HOMOZYGOTE; INFERTILITY, MALE; LAMININ; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, MUTANT STRAINS; MICROSCOPY, ELECTRON; RECEPTORS, G-PROTEIN-COUPLED; RETE TESTIS; SODIUM-HYDROGEN ANTIPORTER; SPERM MOTILITY; SURVIVAL ANALYSIS; TESTIS;

MUS;

EID: 33846861518     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.106.054619     Document Type: Article

References (46)

1. Hinton BT, Palladino MA, Rudolph D, Lan ZJ, Labus JC. The role of the epididymis in the protection of spermatozoa. Curr Top Dev Biol 1996; 33:61-102.
2. Jones RC. To store or mature spermatozoa? The primary role of the epididymis. Int J Androl 1999; 22:57-67.
3. Abou-Haila A, Fain-Maurel MA. Regional differences of the proximal part of mouse epididymis: morphological and histochemical characterization. Anat Rec 1984; 209:197-208.
4. Abou-Haila A, Fain-Maurel MA. Postnatal differentiation of the enzymatic activity of the mouse epididymis. Int J Androl 1985; 8:441-458.
5. Drevet JR, Lareyre JJ, Schwaab V, Vernet P, Dufaure JP. The PEA3 protein of the Ets oncogene family is a putative transcriptional modulator of the mouse epididymis-specific glutathione peroxidase gene gpx5. Mol Reprod Dev 1998; 49:131-140.
6. Suzuki K, Lareyre JJ, Sanchez D, Gutierrez G, Araki Y, Matusik RJ, Orgebin-Crist MC. Molecular evolution of epididymal lipocalin genes localized on mouse chromosome 2. Gene 2004; 339:49-59.
7. Vemet P, Faure J, Dufaure JP, Drevet JR. Tissue and developmental distribution, dependence upon testicular factors and attachment to spermatozoa of GPX5, a murine epididymis-specific glutathione peroxidase. Mol Reprod Dev 1997; 47:87-98.
8. Hsia N, Cornwall GA. Cres2 and Cres3: new members of the cystatin-related epididymal spermatogenic subgroup of family 2 cystatins. Endocrinology 2003; 144:909-915.
9. Fox SA, Yang L, Hinton BT. Identifying putative contraceptive targets by dissecting signal transduction networks in the epididymis using an in vivo electroporation (electrotransfer) approach. Mol Cell Endocrinol 2006; 250:196-200.
10. Ezer N, Robaire B. Gene expression is differentially regulated in the epididymis after orchidectomy. Endocrinology 2003; 144:975-988.
11. Behringer RR, Finegold MJ, Cate RL. Mullerian-inhibiting substance function during mammalian sexual development. Cell 1994; 79:415-425.
12. Yamashita S. Localization of estrogen and androgen receptors in male reproductive tissues of mice and rats. Anat Rec A Discov Mol Cell Evol Biol 2004; 279:768-778.
13. Hess RA. Estrogen in the adult male reproductive tract: a review. Reprod Biol Endocrinol 2003; 1:52.
14. Hess RA, Bunick D, Lee KH, Bahr J, Taylor JA, Korach KS, Lubahn DB. A role for oestrogens in the male reproductive system. Nature 1997; 390:509-512.
15. Zhou Q, Clarke L, Nie R, Cames K, Lai LW, Lien YH, Verkman A, Lubahn D, Fisher JS, Katzenellenbogen BS, Hess RA. Estrogen action and male fertility: roles of the sodium/hydrogen exchanger-3 and fluid reabsorption in reproductive tract function. Proc Natl Acad Sci U S A 2001; 98:14132-14137.
16. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA, Smithies O. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci USA 1998; 95:15677-15682.
17. Couse JF, Hewitt SC, Bunch DO, Sar M, Walker VR, Davis BJ, Korach KS. Postnatal sex reversal of the ovaries in mice lacking estrogen receptors alpha and beta. Science 1999; 286:2328-2331.
18. Higgins SJ, Young P, Cunha GR. Induction of functional cytodifferentiation in the epithelium of tissue recombinants. II. Instructive induction of Wolffian duct epithelia by neonatal seminal vesicle mesenchyme. Development 1989; 106:235-250.
19. Zhao GQ, Liaw L, Hogan BL. Bone morphogenetic protein 8A plays a role in the maintenance of spermatogenesis and the integrity of the epididymis. Development 1998; 125:1103-1112.
20. Zhao GQ, Chen YX, Liu XM, Xu Z, Qi X. Mutation in Bmp7 exacerbates the phenotype of Bmp8a mutants in spermatogenesis and epididymis. Dev Biol 2001; 240:212-222.
21. Hu J, Chen YX, Wang D, Qi X, Li TG, Hao J, Mishina Y, Garbers DL, Zhao GQ. Developmental expression and function of Bmp4 in spermatogenesis and in maintaining epididymal integrity. Dev Biol 2004; 276:158-171.
22. Chen MY, Carpenter D, Zhao GQ. Expression of bone morphogenetic protein 7 in murine epididymis is developmentally regulated. Biol Reprod 1999; 60:1503-1508.
23. Liu ZZ, Wada J, Kumar A, Carone FA, Takahashi M, Kanwar YS. Comparative role of phosphotyrosine kinase domains of c-ros and c-ret protooncogenes in metanephric development with respect to growth factors and matrix morphogens. Dev Biol 1996; 178:133-148.
24. Sonnenberg-Riethmacher E, Walter B, Riethmacher D, Godecke S, Birchmeier C. The c-ros tyrosine kinase receptor controls regionalization and differentiation of epithelial cells in the epididymis. Genes Dev 1996; 10:1184-1193.
25. Mazerbourg S, Bouley DM, Sudo S, Klein CA, Zhang JV, Kawamura K, Goodrich LV, Rayburn H, Tessier-Lavigne M, Hsueh AJ. Leucine-rich repeat-containing, G protein-coupled receptor 4 null mice exhibit intrauterine growth retardation associated with embryonic and perinatal lethality. Mol Endocrinol 2004; 18:2241-2254.
26. Mendive F, Laurent P, Van Schoore G, Skarnes W, Pochet R, Vassart G. Defective postnatal development of the male reproductive tract in LGR4 knockout mice. Dev Biol 2006; 290:421-434.
27. Hsu SY. New insights into the evolution of the relaxin-LGR signaling system. Trends Endocrinol Metab 2003; 14:303-309.
28. Taniwaki T, Haruna K, Nakamura H, Sekimoto T, Oike Y, Imaizumi T, Saito F, Muta M, Soejima Y, Utoh A, Nakagata N, Araki M, et al. Characterization of an exchangeable gene trap using pU-17 carrying a stop codon-beta geo cassette. Dev Growth Differ 2005; 47:163-172.
29. Sztein JM, Farley JS, Mobraaten LE. In vitro fertilization with cryopreserved inbred mouse sperm. Biol Reprod 2000; 63:1774-1780.
30. Schoore GV, Mendive F, Pochet R, Vassart G. Expression pattern of the orphan receptor LGR4/GPR48 gene in the mouse. Histochem Cell Biol 2005; 124:35-50.
31. Avram CE, Cooper TG. Development of the caput epididymidis studied by expressed proteins (a glutamate transporter, a lipocalin and beta-galactosidase) in the c-ros knockout and wild-type mice with prepubertally ligated efferent ducts. Cell Tissue Res 2004; 317:23-34.
32. Fouchecourt S, Lareyre JJ, Chaurand P, DaGue BB, Suzuki K, Ong DE, Olson GE, Matusik RJ, Caprioli RM, Orgebin-Crist MC. Identification, immunolocalization, regulation, and postnatal development of the lipocalin EP17 (epididymal protein of 17 kilodaltons) in the mouse and rat epididymis. Endocrinology 2003; 144:887-900.
33. Agarwal A, Hoffer AP. Ultrastructural studies on the development of the blood-epididymis barrier in immature rats. J Androl 1989; 10:425-431.
34. Timpl R, Brown JC. Supramolecular assembly of basement membranes. BioEssays 1996; 18:123-132.
35. Cooper TG. Role of the epididymis in mediating changes in the male gamete during maturation. Adv Exp Med Biol 1995; 377:87-101.
36. Yeung CH, Sonnenberg-Riethmacher E, Cooper TG. Infertile spermatozoa of c-ros tyrosine kinase receptor knockout mice show flagellar angulation and maturational defects in cell volume regulatory mechanisms. Biol Reprod 1999; 61:1062-1069.
37. Zhou Q, Nie R, Prins GS, Saunders PT, Katzenellenbogen BS, Hess RA. Localization of androgen and estrogen receptors in adult male mouse reproductive tract. J Androl 2002; 23:870-881.
38. Streuli C. Extracellular matrix remodelling and cellular differentiation. Curr Opin Cell Biol 1999; 11:634-640.
39. Pohl M, Sakurai H, Bush KT, Nigam SK. Matrix metalloproteinases and their inhibitors regulate in vitro ureteric bud branching morphogenesis. Am J Physiol Renal Physiol 2000; 279:F891-900.
40. Nee LE, McMorrow T, Campbell E, Slattery C, Ryan MP. TNF-alpha and IL-1 beta-mediated regulation of MMP-9 and TlMP-1 in renal proximal tubular cells. Kidney Int 2004; 66:1376-1386.
41. zum Gottesberge AM, Felix H. Abnormal basement membrane in the inner ear and the kidney of the Mpv17-/- mouse strain: ultrastructural and immunohistochemical investigations. Histochem Cell Biol 2005; 124:507-516.
42. Reuter A, Nestl A, Zwacka RM, Tuckermann J, Waldherr R, Wagner EM, Hoyhtya M, Meyer zum Gottesberge AM, Angel P, Weiher H. Expression of the recessive glomerulosclerosis gene Mpv17 regulates MMP-2 expression in fibroblasts, the kidney, and the inner ear of mice. Mol Biol Cell 1998; 9:1675-1682.
43. Novaro V, Roskelley CD, Bissell MJ. Collagen-IV and laminin-1 regulate estrogen receptor alpha expression and function in mouse mammary epithelial cells. J Cell Sci 2003; 116:2975-2986.
44. Novaro V, Radisky DC, Ramos Castro NE, Weisz A, Bissell MJ. Malignant mammary cells acquire independence from extracellular context for regulation of estrogen receptor alpha. Clin Cancer Res 2004; 10:402S-409S.
45. Mendive FM, Van Loy T, Claeysen S, Poels J, Williamson M, Hauser F, Grimmelikhuijzen CJ, Vassart G, Vanden Broeck J. Drosophila molting neurohormone bursicon is a heterodimer and the natural agonist of the orphan receptor DLGR2. FEBS Lett 2005; 579:2171-2176.
46. Luo CW, Dewey EM, Sudo S, Ewer J, Hsu SY, Honegger HW, Hsueh AJ. Bursicon, the insect cuticle-hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2. Proc Natl Acad Sci U S A 2005; 102:2820-2825.