Hematopoietic prostaglandin D synthase (H-Pgds) is expressed in the early embryonic gonad and participates to the initial nuclear translocation of the SOX9 protein

Developmental Dynamics

Volumn 240, Issue 10, 2011, Pages 2335-2343

  Moniot, Brigitte ^a   Farhat, Andalib ^a   Aritake, Kosuke ^b   Declosmenil, Faustine ^a   Nef, Serge ^c   Eguchi, Naomi ^b   Urade, Yoshihiro ^b   Poulat, Francis ^a   Boizet Bonhoure, Brigitte ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

^b OSAKA BIOSCIENCE INSTITUTE   (Japan)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Pgds; Prostaglandin D2; Sertoli cell; SOX9; Subcellular localization

Indexed keywords

HEMATOPOIETIC PROSTAGLANDIN D SYNTHASE; PROSTAGLANDIN D SYNTHASE; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; EMBRYO; ENZYME ACTIVITY; FEMALE; GERM CELL; GONAD DEVELOPMENT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SERTOLI CELL; SOMATIC CELL;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; FEMALE; GONADS; HUMANS; ISOMERASES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROSTAGLANDIN D2; SERTOLI CELLS; SOX9 TRANSCRIPTION FACTOR;

MAMMALIA;

EID: 80052966433     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22726     Document Type: Article

References (34)

1. Adams IR, McLaren A. 2002. Sexually dimorphic development of mouse primordial germ cells: switching from oogenesis to spermatogenesis. Development 129: 1155-1164.
2. Argentaro A, Sim H, Kelly S, Preiss S, Clayton A, Jans DA, Harley VR. 2003. A SOX9 defect of calmodulin-dependent nuclear import in campomelic dysplasia/autosomal sex reversal. J Biol Chem 278: 33839-33847.
3. Aritake K, Kado Y, Inoue T, Miyano M, Urade Y. 2006. Structural and functional characterization of HQL-79, an orally selective inhibitor of human hematopoietic prostaglandin D synthase. J Biol Chem 281: 15277-15286.
4. Bullejos M, Koopman P. 2005. Delayed Sry and Sox9 expression in developing mouse gonads underlies B6-Y(DOM) sex reversal. Dev Biol 278: 473-481.
5. de Santa Barbara P, Moniot B, Poulat F, Berta P. 2000. Expression and subcellular localization of SF-1, SOX9, WT1, and AMH proteins during early human testicular development. Dev Dyn 217: 293-298.
6. de Santa Barbara P, Mejean C, Moniot B, Malcles MH, Berta P, Boizet-Bonhoure B. 2001. Steroidogenic factor-1 contributes to the cyclic-adenosine monophosphate down-regulation of human SRY gene expression. Biol Reprod 64: 775-783.
7. Farhat A, Philibert P, Sultan C, Poulat F, Boizet-Bonhoure B. 2011. Hematopoietic-Prostaglandin D2 synthase through PGD2 production is involved in the adult ovarian physiology. J Ovarian Res 4: 3.
8. Gasca S, Canizares J, De Santa Barbara P, Mejean C, Poulat F, Berta P, Boizet-Bonhoure B. 2002. A nuclear export signal within the high mobility group domain regulates the nucleocytoplasmic translocation of SOX9 during sexual determination. Proc Natl Acad Sci U S A 99: 11199-11204.
9. Guerquin MJ, Duquenne C, Lahaye JB, Tourpin S, Habert R, Livera G. 2010. New testicular mechanisms involved in the prevention of fetal meiotic initiation in mice. Dev Biol 346: 320-330.
10. Hacker A, Capel B, Goodfellow P, Lovell-Badge R. 1995. Expression of Sry, the mouse sex determining gene. Development 121: 1603-1614.
11. Harley VR, Layfield S, Mitchell CL, Forwood JK, John AP, Briggs LJ, McDowall SG, Jans DA. 2003. Defective importin beta recognition and nuclear import of the sex-determining factor SRY are associated with XY sex-reversing mutations. Proc Natl Acad Sci U S A 100: 7045-7050.
12. Hiramatsu R, Matoba S, Kanai-Azuma M, Tsunekawa N, Katoh-Fukui Y, Kurohmaru M, Morohashi K, Wilhelm D, Koopman P, Kanai Y. 2009. A critical time window of Sry action in gonadal sex determination in mice. Development 136: 129-138.
13. Kanaoka Y, Urade Y. 2003. Hematopoietic prostaglandin D synthase. Prostaglandins Leukot Essent Fatty Acids 69: 163-167.
14. Kim Y, Kobayashi A, Sekido R, Dinapoli L, Brennan J, Chaboissier MC, Poulat F, Behringer RR, Lovell-Badge R, Capel B. 2006. Fgf9 and wnt4 act as antagonistic signals to regulate Mammalian sex determination. PLoS Biol 4: e187.
15. Malki S, Berta P, Poulat F, Boizet-Bonhoure B. 2005a. Cytoplasmic retention of the sex-determining factor SOX9 via the microtubule network. Exp Cell Res 309: 468-475.
16. Malki S, Nef S, Notarnicola C, Thevenet L, Gasca S, Mejean C, Berta P, Poulat F, Boizet-Bonhoure B. 2005b. Prostaglandin D2 induces nuclear import of the sex-determining factor SOX9 via its cAMP-PKA phosphorylation. EMBO J 24: 1798-1809.
17. Matsushita N, Aritake K, Takada A, Hizue M, Hayashi K, Mitsui K, Hayashi M, Hirotsu I, Kimura Y, Tani T, Nakajima H. 1998. Pharmacological studies on the novel antiallergic drug HQL-79: II. Elucidation of mechanisms for antiallergic and antiasthmatic effects. Jpn J Pharmacol 78: 11-22.
18. Michimata T, Tsuda H, Sakai M, Fujimura M, Nagata K, Nakamura M, Saito S. 2002. Accumulation of CRTH2-positive T-helper 2 and T-cytotoxic 2 cells at implantation sites of human decidua in a prostaglandin D(2)-mediated manner. Mol Hum Reprod 8: 181-187.
19. Mohri I, Taniike M, Taniguchi H, Kanekiyo T, Aritake K, Inui T, Fukumoto N, Eguchi N, Kushi A, Sasai H, Kanaoka Y, Ozono K, Narumiya S, Suzuki K, Urade Y. 2006. Prostaglandin D2-mediated microglia/astrocyte interaction enhances astrogliosis and demyelination in twitcher. J Neurosci 26: 4383-4393.
20. Moniot B, Boizet-Bonhoure B, Poulat F. 2008. Male specific expression of lipocalin-type prostaglandin D synthase (cPTGDS) during chicken gonadal differentiation: relationship with cSOX9. Sex Dev 2: 96-103.
21. Moniot B, Declosmenil F, Barrionuevo F, Scherer G, Aritake K, Malki S, Marzi L, Cohen-Solal A, Georg I, Klattig J, Englert C, Kim Y, Capel B, Eguchi N, Urade Y, Boizet-Bonhoure B, Poulat F. 2009. The PGD2 pathway, independently of FGF9, amplifies SOX9 activity in Sertoli cells during male sexual differentiation. Development 136: 1813-1821.
22. Nef S, Schaad O, Stallings NR, Cederroth CR, Pitetti JL, Schaer G, Malki S, Dubois-Dauphin M, Boizet-Bonhoure B, Descombes P, Parker KL, Vassalli JD. 2005. Gene expression during sex determination reveals a robust female genetic program at the onset of ovarian development. Dev Biol 287: 361-377.
23. Notarnicola C, Malki S, Berta P, Poulat F, Boizet-Bonhoure B. 2006. Transient expression of SOX9 protein during follicular development in the adult mouse ovary. Gene Expr Patterns 6: 695-702.
24. Rossi P, Dolci S, Albanesi C, Grimaldi P, Geremia R. 1993. Direct evidence that the mouse sex-determining gene Sry is expressed in the somatic cells of male fetal gonads and in the germ cell line in the adult testis. Mol Reprod Dev 34: 369-373.
25. Schell C, Frungieri MB, Albrecht M, Gonzalez-Calvar SI, Kohn FM, Calandra RS, Mayerhofer A. 2007. A Prostaglandin D2 system in the human testis. Fertil Steril 88: 233-236.
26. Sekido R, Lovell-Badge R. 2008. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453: 930-934.
27. Sim H, Argentaro A, Czech DP, Bagheri-Fam S, Sinclair AH, Koopman P, Boizet-Bonhoure B, Poulat F, Harley VR. 2011. Inhibition of SRY-calmodulin complex formation induces ectopic expression of ovarian cell markers in developing XY gonads. Endocrinology 152: 2883-2893.
28. Stallings NR, Hanley NA, Majdic G, Zhao L, Bakke M, Parker KL. 2002. Development of a transgenic green fluorescent protein lineage marker for steroidogenic factor 1. Endocr Res 28: 497-504.
29. Sudbeck P, Scherer G. 1997. Two independent nuclear localization signals are present in the DNA-binding high-mobility group domains of SRY and SOX9. J Biol Chem 272: 27848-27852.
30. Svingen T, Spiller CM, Kashimada K, Harley VR, Koopman P. 2009. Identification of suitable normalizing genes for quantitative real-time RT-PCR analysis of gene expression in fetal mouse gonads. Sex Dev 3: 194-204.
31. Trivedi SG, Newson J, Rajakariar R, Jacques TS, Hannon R, Kanaoka Y, Eguchi N, Colville-Nash P, Gilroy DW. 2006. Essential role for hematopoietic prostaglandin D2 synthase in the control of delayed type hypersensitivity. Proc Natl Acad Sci U S A 103: 5179-5184.
32. Wilhelm D, Martinson F, Bradford S, Wilson MJ, Combes AN, Beverdam A, Bowles J, Mizusaki H, Koopman P. 2005. Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev Biol 287: 111-124.
33. Wilhelm D, Hiramatsu R, Mizusaki H, Widjaja L, Combes AN, Kanai Y, Koopman P. 2007a. SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J Biol Chem 282: 10553-10560.
34. Wilhelm D, Palmer S, Koopman P. 2007b. Sex determination and gonadal development in mammals. Physiol Rev 87: 1-28.