Gadd45γ and Map3k4 Interactions Regulate Mouse Testis Determination via p38 MAPK-Mediated Control of Sry Expression

Developmental Cell

Volumn 23, Issue 5, 2012, Pages 1020-1031

  Warr, Nick ^a   Carre, Gwenn Aël ^a   Siggers, Pam ^a   Faleato, Jessica Vitos ^c   Brixey, Rachel ^a   Pope, Madeleine ^a   Bogani, Debora ^a,g   Childers, Melissa ^d   Wells, Sara ^b   Scudamore, Cheryl L ^e   Tedesco, Marianna ^c   del Barco Barrantes, Ivan ^c   Nebreda, Angel R ^c   Trainor, Paul A ^d,f   Greenfield, Andy ^a  

^a MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

^b Medical Research Council Harwell Institute   (United Kingdom)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^d STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^e ROYAL VETERINARY COLLEGE   (United Kingdom)

^f UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45 GAMMA; MAP3K4 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN; TESTIS DETERMINING FACTOR; TRANSCRIPTION FACTOR GATA 4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE OVEREXPRESSION; GENETIC ANALYSIS; KARYOTYPE 46,XY; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEX DETERMINATION; SEX TRANSFORMATION; SIGNAL TRANSDUCTION; SOMATIC CELL; TESTIS;

ANIMALS; CARRIER PROTEINS; DNA METHYLATION; FEMALE; GATA4 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, SRY; GONADAL DYSGENESIS, 46,XY; MALE; MAP KINASE KINASE KINASE 4; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 11; MITOGEN-ACTIVATED PROTEIN KINASE 14; MODELS, BIOLOGICAL; SEX DETERMINATION PROCESSES; SEX-DETERMINING REGION Y PROTEIN; TESTIS;

MAMMALIA; MUS;

EID: 84869083497     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.09.016     Document Type: Article

References (44)

1. Abell A.N., Jordan N.V., Huang W., Prat A., Midland A.A., Johnson N.L., Granger D.A., Mieczkowski P.A., Perou C.M., Gomez S.M., et al. MAP3K4/CBP-regulated H2B acetylation controls epithelial-mesenchymal transition in trophoblast stem cells. Cell Stem Cell 2011, 8:525-537.
2. Adams R.H., Porras A., Alonso G., Jones M., Vintersten K., Panelli S., Valladares A., Perez L., Klein R., Nebreda A.R. Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development. Mol. Cell 2000, 6:109-116.
3. Albrecht K.H., Eicher E.M. Evidence that Sry is expressed in pre-Sertoli cells and Sertoli and granulosa cells have a common precursor. Dev. Biol. 2001, 240:92-107.
4. Barreto G., Schäfer A., Marhold J., Stach D., Swaminathan S.K., Handa V., Döderlein G., Maltry N., Wu W., Lyko F., Niehrs C. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 2007, 445:671-675.
5. Beardmore V.A., Hinton H.J., Eftychi C., Apostolaki M., Armaka M., Darragh J., McIlrath J., Carr J.M., Armit L.J., Clacher C., et al. Generation and characterization of p38beta (MAPK11) gene-targeted mice. Mol. Cell. Biol. 2005, 25:10454-10464.
6. Bogani D., Siggers P., Brixey R., Warr N., Beddow S., Edwards J., Williams D., Wilhelm D., Koopman P., Flavell R.A., et al. Loss of mitogen-activated protein kinase kinase kinase 4 (MAP3K4) reveals a requirement for MAPK signalling in mouse sex determination. PLoS Biol. 2009, 7:e1000196.
7. Bouma G.J., Washburn L.L., Albrecht K.H., Eicher E.M. Correct dosage of Fog2 and Gata4 transcription factors is critical for fetal testis development in mice. Proc. Natl. Acad. Sci. USA 2007, 104:14994-14999.
8. Bulynko Y.A., Hsing L.C., Mason R.W., Tremethick D.J., Grigoryev S.A. Cathepsin L stabilizes the histone modification landscape on the Y chromosome and pericentromeric heterochromatin. Mol. Cell. Biol. 2006, 26:4172-4184.
9. Charron F., Tsimiklis G., Arcand M., Robitaille L., Liang Q., Molkentin J.D., Meloche S., Nemer M. Tissue-specific GATA factors are transcriptional effectors of the small GTPase RhoA. Genes Dev. 2001, 15:2702-2719.
10. Chi H., Lu B., Takekawa M., Davis R.J., Flavell R.A. GADD45beta/GADD45gamma and MEKK4 comprise a genetic pathway mediating STAT4-independent IFNgamma production in T cells. EMBO J. 2004, 23:1576-1586.
11. Cuadrado A., Nebreda A.R. Mechanisms and functions of p38 MAPK signalling. Biochem. J. 2010, 429:403-417.
12. Cuadrado A., Corrado N., Perdiguero E., Lafarga V., Muñoz-Canoves P., Nebreda A.R. Essential role of p18Hamlet/SRCAP-mediated histone H2A.Z chromatin incorporation in muscle differentiation. EMBO J. 2010, 29:2014-2025.
13. del Barco Barrantes I., Coya J.M., Maina F., Arthur J.S., Nebreda A.R. Genetic analysis of specific and redundant roles for p38alpha and p38beta MAPKs during mouse development. Proc. Natl. Acad. Sci. USA 2011, 108:12764-12769.
14. Ewen K., Jackson A., Wilhelm D., Koopman P. A male-specific role for p38 mitogen-activated protein kinase in germ cell sex differentiation in mice. Biol. Reprod. 2010, 83:1005-1014.
15. Ferreiro I., Barragan M., Gubern A., Ballestar E., Joaquin M., Posas F. The p38 SAPK is recruited to chromatin via its interaction with transcription factors. J. Biol. Chem. 2010, 285:31819-31828.
16. Fornace A.J., Alamo I., Hollander M.C. DNA damage-inducible transcripts in mammalian cells. Proc. Natl. Acad. Sci. USA 1988, 85:8800-8804.
17. Gardiner W.J., Teboul L. Overexpression transgenesis in mouse: pronuclear injection. Methods Mol. Biol. 2009, 561:111-126.
18. Gerwins P., Blank J.L., Johnson G.L. Cloning of a novel mitogen-activated protein kinase kinase kinase, MEKK4, that selectively regulates the c-Jun amino terminal kinase pathway. J. Biol. Chem. 1997, 272:8288-8295.
19. Gierl M.S., Gruhn W.H., von Seggern A., Maltry N., Niehrs C. Gadd45 g functions in male sex determination by promoting p38 signaling and Sry expression. Dev. Cell 2012, 23. Published online October 25, 2012. 10.1016/j.devcel.2012.09.016.
20. Hayashi S., Kunisada T., Ogawa M., Yamaguchi K., Nishikawa S. Exon skipping by mutation of an authentic splice site of c-kit gene in W/W mouse. Nucleic Acids Res. 1991, 19:1267-1271.
21. Hiramatsu R., Matoba S., Kanai-Azuma M., Tsunekawa N., Katoh-Fukui Y., Kurohmaru M., Morohashi K.I., Wilhelm D., Koopman P., Kanai Y. A critical time window of Sry action in gonadal sex determination in mice. Development 2009, 136:129-138.
22. Hoffmeyer A., Piekorz R., Moriggl R., Ihle J.N. Gadd45gamma is dispensable for normal mouse development and T-cell proliferation. Mol. Cell. Biol. 2001, 21:3137-3143.
23. Hollander M.C., Fornace A.J. Genomic instability, centrosome amplification, cell cycle checkpoints and Gadd45a. Oncogene 2002, 21:6228-6233.
24. Karl J., Capel B. Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev. Biol. 1998, 203:323-333.
25. Kim Y., Kobayashi A., Sekido R., DiNapoli L., Brennan J., Chaboissier M.C., Poulat F., Behringer R.R., Lovell-Badge R., Capel B. Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol. 2006, 4:e187.
26. Koopman P., Gubbay J., Vivian N., Goodfellow P., Lovell-Badge R. Male development of chromosomally female mice transgenic for Sry. Nature 1991, 351:117-121.
27. Liang Q., Wiese R.J., Bueno O.F., Dai Y.S., Markham B.E., Molkentin J.D. The transcription factor GATA4 is activated by extracellular signal-regulated kinase 1- and 2-mediated phosphorylation of serine 105 in cardiomyocytes. Mol. Cell. Biol. 2001, 21:7460-7469.
28. Lu B., Yu H., Chow C., Li B., Zheng W., Davis R.J., Flavell R.A. GADD45gamma mediates the activation of the p38 and JNK MAP kinase pathways and cytokine production in effector TH1 cells. Immunity 2001, 14:583-590.
29. Miyake Z., Takekawa M., Ge Q., Saito H. Activation of MTK1/MEKK4 by GADD45 through induced N-C dissociation and dimerization-mediated trans autophosphorylation of the MTK1 kinase domain. Mol. Cell. Biol. 2007, 27:2765-2776.
30. Niehrs C., Schäfer A. Active DNA demethylation by Gadd45 and DNA repair. Trends Cell Biol. 2012, 22:220-227.
31. Nishino K., Hattori N., Tanaka S., Shiota K. DNA methylation-mediated control of Sry gene expression in mouse gonadal development. J. Biol. Chem. 2004, 279:22306-22313.
32. Pearlman A., Loke J., Le Caignec C., White S., Chin L., Friedman A., Warr N., Willan J., Brauer D., Farmer C., et al. Mutations in MAP3K1 cause 46,XY disorders of sex development and implicate a common signal transduction pathway in human testis determination. Am. J. Hum. Genet. 2010, 87:898-904.
33. Rai K., Huggins I.J., James S.R., Karpf A.R., Jones D.A., Cairns B.R. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 2008, 135:1201-1212.
34. Russell E.S. Hereditary anemias of the mouse: a review for geneticists. Adv. Genet. 1979, 20:357-459.
35. Sabio G., Arthur J.S., Kuma Y., Peggie M., Carr J., Murray-Tait V., Centeno F., Goedert M., Morrice N.A., Cuenda A. p38gamma regulates the localisation of SAP97 in the cytoskeleton by modulating its interaction with GKAP. EMBO J. 2005, 24:1134-1145.
36. Schmahl J., Capel B. Cell proliferation is necessary for the determination of male fate in the gonad. Dev. Biol. 2003, 258:264-276.
37. Sekido R., Lovell-Badge R. Sex determination and SRY: down to a wink and a nudge?. Trends Genet. 2009, 25:19-29.
38. Takekawa M., Saito H. A family of stress-inducible GADD45-like proteins mediate activation of the stress-responsive MTK1/MEKK4 MAPKKK. Cell 1998, 95:521-530.
39. Takekawa M., Posas F., Saito H. A human homolog of the yeast Ssk2/Ssk22 MAP kinase kinase kinases, MTK1, mediates stress-induced activation of the p38 and JNK pathways. EMBO J. 1997, 16:4973-4982.
40. Tenhunen O., Sármán B., Kerkelä R., Szokodi I., Papp L., Tóth M., Ruskoaho H. Mitogen-activated protein kinases p38 and ERK 1/2 mediate the wall stress-induced activation of GATA-4 binding in adult heart. J. Biol. Chem. 2004, 279:24852-24860.
41. Tevosian S.G., Albrecht K.H., Crispino J.D., Fujiwara Y., Eicher E.M., Orkin S.H. Gonadal differentiation, sex determination and normal Sry expression in mice require direct interaction between transcription partners GATA4 and FOG2. Development 2002, 129:4627-4634.
42. Warr N., Greenfield A. The molecular and cellular basis of gonadal sex reversal in mice and humans. WIREs Dev Biol 2012, 1:559-577.
43. Warr N., Siggers P., Bogani D., Brixey R., Pastorelli L., Yates L., Dean C.H., Wells S., Satoh W., Shimono A., Greenfield A. Sfrp1 and Sfrp2 are required for normal male sexual development in mice. Dev. Biol. 2009, 326:273-284.
44. Winter-Vann A.M., Johnson G.L. Integrated activation of MAP3Ks balances cell fate in response to stress. J. Cell. Biochem. 2007, 102:848-858.