Cited2 is required in trophoblasts for correct placental capillary patterning

Developmental Biology

Volumn 392, Issue 1, 2014, Pages 62-79

  Moreau, Julie L M ^a   Artap, Stanley T ^b,d   Shi, Hongjun ^a   Chapman, Gavin ^a,b   Leone, Gustavo ^c   Sparrow, Duncan B ^a,b   Dunwoodie, Sally L ^a,b  

^a VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c OHIO STATE UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cited2; Mouse; PDGF signaling; Placenta; Trophoblast; Vasculature

Indexed keywords

CRE RECOMBINASE; MONOCARBOXYLATE TRANSPORTER 4; PEPTIDES AND PROTEINS; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN CITED2; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAPILLARY; CELLULAR DISTRIBUTION; CITED2 GENE; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; EXTRA EMBRYONIC MESODERM; FEMALE; FETUS WEIGHT; GENE DELETION; GIANT CELL; INTRAUTERINE GROWTH RETARDATION; MALE; MESODERM; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SURVIVAL; SYNCYTIOTROPHOBLAST; TROPHECTODERM; TROPHOBLAST; VASCULARIZATION;

CITED2; MOUSE; PDGF SIGNALING; PLACENTA; TROPHOBLAST; VASCULATURE;

ACTINS; ANIMALS; ANTIGENS, CD31; BODY PATTERNING; CAPILLARIES; CARRIER PROTEINS; EMBRYONIC DEVELOPMENT; FEMALE; GENE DELETION; MICE; MICE, INBRED C57BL; MONOCARBOXYLIC ACID TRANSPORTERS; MUSCLE PROTEINS; NEOVASCULARIZATION, PHYSIOLOGIC; PERICYTES; PLACENTA; PLACENTAL CIRCULATION; PLATELET-DERIVED GROWTH FACTOR; PREGNANCY; PROTO-ONCOGENE PROTEINS C-SIS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; REPRESSOR PROTEINS; SYMPORTERS; TRANS-ACTIVATORS; TROPHOBLASTS;

EID: 84901920145     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.04.023     Document Type: Article

References (60)

1. Adamson S.L., Lu Y., Whiteley K.J., Holmyard D., Hemberger M., Pfarrer C., Cross J.C. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev. Biol. 2002, 250:358-373.
2. Arora R., Papaioannou V.E. The murine allantois: a model system for the study of blood vessel formation. Blood 2012, 120:2562-2572.
3. Bakker W.J., Harris I.S., Mak T.W. FOXO3a is activated in response to hypoxic stress and inhibits HIF1-induced apoptosis via regulation of CITED2. Mol. Cell 2007, 28:941-953.
4. Bamforth S.D., Braganca J., Eloranta J.J., Murdoch J.N., Marques F.I., Kranc K.R., Farza H., Henderson D.J., Hurst H.C., Bhattacharya S. Cardiac malformations, adrenal agenesis, neural crest defects and exencephaly in mice lacking Cited2, a new Tfap2 co-activator. Nat. Genet. 2001, 29:469-474.
5. Bamforth S.D., Braganca J., Farthing C.R., Schneider J.E., Broadbent C., Michell A.C., Clarke K., Neubauer S., Norris D., Brown N.A., Anderson R.H., Bhattacharya S. Cited2 controls left-right patterning and heart development through a Nodal-Pitx2c pathway. Nat. Genet. 2004, 36:1189-1196.
6. Barbera J.P., Rodriguez T.A., Greene N.D., Weninger W.J., Simeone A., Copp A.J., Beddington R.S., Dunwoodie S. Folic acid prevents exencephaly in Cited2 deficient mice. Hum. Mol. Genet. 2002, 11:283-293.
7. Bhattacharya S., Michels C.L., Leung M.K., Arany Z.P., Kung A.L., Livingston D.M. Functional role of p35srj, a novel p300/CBP binding protein, during transactivation by HIF-1. Genes Dev. 1999, 13:64-75.
8. Bjarnegard M., Enge M., Norlin J., Gustafsdottir S., Fredriksson S., Abramsson A., Takemoto M., Gustafsson E., Fassler R., Betsholtz C. Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 2004, 131:1847-1857.
9. Braganca J., Eloranta J.J., Bamforth S.D., Ibbitt J.C., Hurst H.C., Bhattacharya S. Physical and functional interactions among AP-2 transcription factors, p300/CREB-binding protein, and CITED2. J. Biol. Chem. 2003, 278:16021-16029.
10. Chen Y., Carlson E.C., Chen Z.Y., Hamik A., Jain M.K., Dunwoodie S.L., Yang Y.C. Conditional deletion of Cited2 results in defective corneal epithelial morphogenesis and maintenance. Dev. Biol. 2009, 334:243-252.
11. Chen Y., Doughman Y.Q., Gu S., Jarrell A., Aota S., Cvekl A., Watanabe M., Dunwoodie S.L., Johnson R.S., van Heyningen V., Kleinjan D.A., Beebe D.C., Yang Y.C. Cited2 is required for the proper formation of the hyaloid vasculature and for lens morphogenesis. Development 2008, 135:2939-2948.
12. Chen Y., Haviernik P., Bunting K.D., Yang Y.C. Cited2 is required for normal hematopoiesis in the murine fetal liver. Blood 2007, 110:2889-2898.
13. Chhabra A., Lechner A.J., Ueno M., Acharya A., Van Handel B., Wang Y., Iruela-Arispe M.L., Tallquist M.D., Mikkola H.K. Trophoblasts regulate the placental hematopoietic niche through PDGF-B signaling. Dev. Cell 2012, 22:651-659.
14. Chou Y.T., Wang H., Chen Y., Danielpour D., Yang Y.C. Cited2 modulates TGF-beta-mediated upregulation of MMP9. Oncogene 2006, 25:5547-5560.
15. Chung A.S., Ferrara N. Developmental and pathological angiogenesis. Annu. Rev. Cell Dev. Biol. 2011, 27:563-584.
16. Colombo S., Kumasaka M., Lobe C., Larue L. Genomic localization of the Z/EG transgene in the mouse genome. Genesis 2010, 48:96-100.
17. Constien R., Forde A., Liliensiek B., Grone H.J., Nawroth P., Hammerling G., Arnold B. Characterization of a novel EGFP reporter mouse to monitor Cre recombination as demonstrated by a Tie2 Cre mouse line. Genesis 2001, 30:36-44.
18. Du J., Chen Y., Li Q., Han X., Cheng C., Wang Z., Danielpour D., Dunwoodie S.L., Bunting K.D., Yang Y.C. HIF-1alpha deletion partially rescues defects of hematopoietic stem cell quiescence caused by Cited2 deficiency. Blood 2012, 119:2789-2798.
19. Du J., Li Q., Tang F., Puchowitz M.A., Fujioka H., Dunwoodie S.L., Danielpour D., Yang Y.C. Cited2 is required for the maintenance of glycolytic metabolism in adult hematopoietic stem cells. Stem Cells Dev. 2014, 23:83-94.
20. Dunwoodie S.L., Rodriguez T.A., Beddington R.S. Msg1 and Mrg1, founding members of a gene family, show distinct patterns of gene expression during mouse embryogenesis. Mech. Dev. 1998, 72:27-40.
21. Enders A.C. A comparative study of the fine structure of the trophoblast in several hemochorial placentas. Am. J. Anat. 1965, 116:29-67.
22. Ferrara N., Carver-Moore K., Chen H., Dowd M., Lu L., O'Shea K.S., Powell-Braxton L., Hillan K.J., Moore M.W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996, 380:439-442.
23. Glenn D.J., Maurer R.A. MRG1 binds to the LIM domain of Lhx2 and may function as a coactivator to stimulate glycoprotein hormone alpha-subunit gene expression. J. Biol. Chem. 1999, 274:36159-36167.
24. Hernandez-Verdun D. Morphogenesis of the syncytium in the mouse placenta. Ultrastructural study. Cell Tissue Res. 1974, 148:381-396.
25. Hu D., Cross J.C. Ablation of Tpbpa-positive trophoblast precursors leads to defects in maternal spiral artery remodeling in the mouse placenta. Dev. Biol. 2011, 358:231-239.
26. Jain R.K. Molecular regulation of vessel maturation. Nat. Med. 2003, 9:685-693.
27. John R., Hemberger M. A placenta for life. Reprod. Biomed. Online 2012, 25:5-11.
28. Koni P.A., Joshi S.K., Temann U.A., Olson D., Burkly L., Flavell R.A. Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J. Exp. Med. 2001, 193:741-754.
29. Kranc K.R., Schepers H., Rodrigues N.P., Bamforth S., Villadsen E., Ferry H., Bouriez-Jones T., Sigvardsson M., Bhattacharya S., Jacobsen S.E., Enver T. Cited2 is an essential regulator of adult hematopoietic stem cells. Cell Stem Cell 2009, 5:659-665.
30. Leveen P., Pekny M., Gebre-Medhin S., Swolin B., Larsson E., Betsholtz C. Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev. 1994, 8:1875-1887.
31. Li Q., Ramirez-Bergeron D.L., Dunwoodie S.L., Yang Y.C. Cited2 gene controls pluripotency and cardiomyocyte differentiation of murine embryonic stem cells through Oct4 gene. J. Biol. Chem. 2012, 287:29088-29100.
32. Lopes Floro K., Artap S.T., Preis J.I., Fatkin D., Chapman G., Furtado M.B., Harvey R.P., Hamada H., Sparrow D.B., Dunwoodie S.L. Loss of Cited2 causes congenital heart disease by perturbing left-right patterning of the body axis. Hum. Mol. Genet. 2011, 20:1097-1110.
33. Lou X., Sun S., Chen W., Zhou Y., Huang Y., Liu X., Shan Y., Wang C. Negative feedback regulation of NF-kappaB action by CITED2 in the nucleus. J. Immunol. 2011, 186:539-548.
34. MacDonald S.T., Bamforth S.D., Braganca J., Chen C.M., Broadbent C., Schneider J.E., Schwartz R.J., Bhattacharya S. A cell-autonomous role of Cited2 in controlling myocardial and coronary vascular development. Eur. Heart J. 2013, 34:2557-2565.
35. Mobasheri A., Oukrif D., Dawodu S.P., Sinha M., Greenwell P., Stewart D., Djamgoz M.B., Foster C.S., Martin-Vasallo P., Mobasheri R. Isoforms of Na+, K+-ATPase in human prostate; specificity of expression and apical membrane polarization. Histol. Histopathol. 2001, 16:141-154.
36. Nagai A., Takebe K., Nio-Kobayashi J., Takahashi-Iwanaga H., Iwanaga T. Cellular expression of the monocarboxylate transporter (MCT) family in the placenta of mice. Placenta 2010, 31:126-133.
37. Novak A., Guo C., Yang W., Nagy A., Lobe C.G. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 2000, 28:147-155.
38. Ohlsson R., Falck P., Hellstrom M., Lindahl P., Bostrom H., Franklin G., Ahrlund-Richter L., Pollard J., Soriano P., Betsholtz C. PDGFB regulates the development of the labyrinthine layer of the mouse fetal placenta. Dev. Biol. 1999, 212:124-136.
39. Preis J.I., Wise N., Solloway M.J., Harvey R.P., Sparrow D.B., Dunwoodie S.L. Generation of conditional Cited2 null alleles. Genesis 2006, 44:579-583.
40. Pritsker M., Ford N.R., Jenq H.T., Lemischka I.R. Genomewide gain-of-function genetic screen identifies functionally active genes in mouse embryonic stem cells. Proc. Natl. Acad. Sci. USA 2006, 103:6946-6951.
41. Qu X., Lam E., Doughman Y.Q., Chen Y., Chou Y.T., Lam M., Turakhia M., Dunwoodie S.L., Watanabe M., Xu B., Duncan S.A., Yang Y.C. Cited2, a coactivator of HNF4alpha, is essential for liver development. EMBO J. 2007, 26:4445-4456.
42. Ribatti D., Nico B., Crivellato E. The role of pericytes in angiogenesis. Int. J. Dev. Biol. 2011, 55:261-268.
43. Rodriguez T.A., Sparrow D.B., Scott A.N., Withington S.L., Preis J.I., Michalicek J., Clements M., Tsang T.E., Shioda T., Beddington R.S., Dunwoodie S.L. Cited1 is required in trophoblasts for placental development and for embryo growth and survival. Mol. Cell Biol. 2004, 24:228-244.
44. Sakai M., Matsumoto M., Tujimura T., Yongheng C., Noguchi T., Inagaki K., Inoue H., Hosooka T., Takazawa K., Kido Y., Yasuda K., Hiramatsu R., Matsuki Y., Kasuga M. CITED2 links hormonal signaling to PGC-1alpha acetylation in the regulation of gluconeogenesis. Nat. Med. 2012, 18:612-617.
45. Shalaby F., Rossant J., Yamaguchi T.P., Gertsenstein M., Wu X.F., Breitman M.L., Schuh A.C. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995, 376:62-66.
46. Simmons D.G., Fortier A.L., Cross J.C. Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev. Biol. 2007, 304:567-578.
47. Simmons D.G., Natale D.R., Begay V., Hughes M., Leutz A., Cross J.C. Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 2008, 135:2083-2091.
48. Soriano P. Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes Dev. 1994, 8:1888-1896.
49. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 1999, 21:70-71.
50. Tang N., Wang L., Esko J., Giordano F.J., Huang Y., Gerber H.P., Ferrara N., Johnson R.S. Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell. 2004, 6:485-495.
51. Tien E.S., Davis J.W., Vanden Heuvel J.P. Identification of the CREB-binding protein/p300-interacting protein CITED2 as a peroxisome proliferator-activated receptor alpha coregulator. J. Biol. Chem. 2004, 279:24053-24063.
52. Viegas M.S., Martins T.C., Seco F., do Carmo A. An improved and cost-effective methodology for the reduction of autofluorescence in direct immunofluorescence studies on formalin-fixed paraffin-embedded tissues. Eur. J. Histochem. 2007, 51:59-66.
53. Vooijs M., Jonkers J., Berns A. A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO Rep. 2001, 2:292-297.
54. Weninger W.J., Lopes Floro K., Bennett M.B., Withington S.L., Preis J.I., Barbera J.P., Mohun T.J., Dunwoodie S.L. Cited2 is required both for heart morphogenesis and establishment of the left-right axis in mouse development. Development 2005, 132:1337-1348.
55. Wenzel P.L., Leone G. Expression of Cre recombinase in early diploid trophoblast cells of the mouse placenta. Genesis 2007, 45:129-134.
56. Withington S.L., Scott A.N., Saunders D.N., Lopes Floro K., Preis J.I., Michalicek J., Maclean K., Sparrow D.B., Barbera J.P., Dunwoodie S.L. Loss of Cited2 affects trophoblast formation and vascularization of the mouse placenta. Dev. Biol. 2006, 294:67-82.
57. Wu Z.Z., Sun N.K., Chao C.C. Knockdown of CITED2 using short-hairpin RNA sensitizes cancer cells to cisplatin through stabilization of p53 and enhancement of p53-dependent apoptosis. J. Cell Physiol. 2011, 226:2415-2428.
58. Xu B., Qu X., Gu S., Doughman Y.Q., Watanabe M., Dunwoodie S.L., Yang Y.C. Cited2 is required for fetal lung maturation. Dev. Biol. 2008, 317:95-105.
59. Yin Z., Haynie J., Yang X., Han B., Kiatchoosakun S., Restivo J., Yuan S., Prabhakar N.R., Herrup K., Conlon R.A., Hoit B.D., Watanabe M., Yang Y.C. The essential role of Cited2, a negative regulator for HIF-1alpha, in heart development and neurulation. Proc. Natl. Acad. Sci. USA 2002, 99:10488-10493.
60. Yokota H., Goldring M.B., Sun H.B. CITED2-mediated regulation of MMP-1 and MMP-13 in human chondrocytes under flow shear. J. Biol. Chem. 2003, 278:47275-47280.