APOBEC2, a selective inhibitor of TGFβsignaling, regulates left-right axis specification during early embryogenesis

Developmental Biology

Volumn 350, Issue 1, 2011, Pages 13-23

  Vonica, Alin ^a,b   Rosa, Alessandro ^a   Arduini, Brigitte L ^a   Brivanlou, Ali H ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

APOBEC2; Left right; Muscle; TGF ; Xenopus

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 2; CYTIDINE DEAMINASE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME ANALYSIS; GENETIC CONSERVATION; MAMMAL CELL; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; XENOPUS; ZEBRA FISH;

DANIO RERIO; MAMMALIA; VERTEBRATA;

EID: 78651227102     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.09.016     Document Type: Article

References (73)

1. Amthor H., Macharia R., Navarrete R., Schuelke M., Brown S.C., Otto A., Voit T., Muntoni F., Vrbova G., Partridge T., Zammit P., Bunger L., Patel K. Lack of myostatin results in excessive muscle growth but impaired force generation. Proc. Natl Acad. Sci. USA 2007, 104:1835-1840.
2. Anant S., Mukhopadhyay D., Sankaranand V., Kennedy S., Henderson J.O., Davidson N.O. ARCD-1, an apobec-1-related cytidine deaminase, exerts a dominant negative effect on C to U RNA editing. Am. J. Physiol. Cell Physiol. 2001, 281:C1904-C1916.
3. Artaza J.N., Bhasin S., Mallidis C., Taylor W., Ma K., Gonzalez-Cadavid N.F. Endogenous expression and localization of myostatin and its relation to myosin heavy chain distribution in C2C12 skeletal muscle cells. J. Cell. Physiol. 2002, 190:170-179.
4. Bell E., Munoz-Sanjuan I., Altmann C.R., Vonica A., Brivanlou A.H. Cell fate specification and competence by Coco, a maternal BMP, TGFbeta and Wnt inhibitor. Development 2003, 130:1381-1389.
5. Bisgrove B.W., Yost H.J. Classification of left-right patterning defects in zebrafish, mice, and humans. Am. J. Med. Genet. 2001, 101:315-323.
6. Bisgrove B.W., Yost H.J. The roles of cilia in developmental disorders and disease. Development 2006, 133:4131-4143.
7. Brand T. Heart development: molecular insights into cardiac specification and early morphogenesis. Dev. Biol. 2003, 258:1-19.
8. Branford W.W., Essner J.J., Yost H.J. Regulation of gut and heart left-right asymmetry by context-dependent interactions between xenopus lefty and BMP4 signaling. Dev. Biol. 2000, 223:291-306.
9. Brannon M., Gomperts M., Sumoy L., Moon R.T., Kimelman D. A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus. Genes Dev. 1997, 11:2359-2370.
10. Chen J.N., Fishman M.C. Zebrafish tinman homolog demarcates the heart field and initiates myocardial differentiation. Development 1996, 122:3809-3816.
11. Cheng S.K., Olale F., Bennett J.T., Brivanlou A.H., Schier A.F. EGF-CFC proteins are essential coreceptors for the TGF-beta signals Vg1 and GDF1. Genes Dev. 2003, 17:31-36.
12. Conticello S.G. The AID/APOBEC family of nucleic acid mutators. Genome Biol. 2008, 9:229.
13. Conticello S.G., Langlois M.A., Yang Z., Neuberger M.S. DNA deamination in immunity: AID in the context of its APOBEC relatives. Adv. Immunol. 2007, 94:37-73.
14. Dale L. Development: morphogen gradients and mesodermal patterning. Curr. Biol. 1997, 7:R698-R700.
15. Dorey K., Hill C.S. A novel Cripto-related protein reveals an essential role for EGF-CFCs in Nodal signalling in Xenopus embryos. Dev. Biol. 2006, 292:303-316.
16. Eimon P.M., Harland R.M. Effects of heterodimerization and proteolytic processing on Derriere and Nodal activity: implications for mesoderm induction in Xenopus. Development 2002, 129:3089-3103.
17. Esguerra C.V., Nelles L., Vermeire L., Ibrahimi A., Crawford A.D., Derua R., Janssens E., Waelkens E., Carmeliet P., Collen D., Huylebroeck D. Ttrap is an essential modulator of Smad3-dependent Nodal signaling during zebrafish gastrulation and left-right axis determination. Development 2007, 134:4381-4393.
18. Essner J.J., Amack J.D., Nyholm M.K., Harris E.B., Yost H.J. Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 2005, 132:1247-1260.
19. Essner J.J., Vogan K.J., Wagner M.K., Tabin C.J., Yost H.J., Brueckner M. Conserved function for embryonic nodal cilia.[see comment]. Nature 2002, 418:37-38.
20. Girgenrath S., Song K., Whittemore L.A. Loss of myostatin expression alters fiber-type distribution and expression of myosin heavy chain isoforms in slow- and fast-type skeletal muscle. Muscle Nerve 2005, 31:34-40.
21. Green J. Morphogen gradients, positional information, and Xenopus: interplay of theory and experiment. Dev. Dyn. 2002, 225:392-408.
22. Gritsman K., Zhang J., Cheng S., Heckscher E., Talbot W.S., Schier A.F. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell 1999, 97:121-132.
23. Gros J., Feistel K., Viebahn C., Blum M., Tabin C.J. Cell movements at Hensen's node establish left/right asymmetric gene expression in the chick. Science 2009, 324:941-944.
24. Harland R., Gerhart J. Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 1997, 13:611-667.
25. Harland R.M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Meth. Cell Biol. 1991, 36:685-695.
26. Hashimoto H., Rebagliati M., Ahmad N., Muraoka O., Kurokawa T., Hibi M., Suzuki T. The Cerberus/Dan-family protein Charon is a negative regulator of Nodal signaling during left-right patterning in zebrafish. Development 2004, 131:1741-1753.
27. Hirokawa N., Tanaka Y., Okada Y., Takeda S. Nodal flow and the generation of left-right asymmetry. Cell 2006, 125:33-45.
28. Howell M., Inman G.J., Hill C.S. A novel Xenopus Smad-interacting forkhead transcription factor (XFast-3) cooperates with XFast-1 in regulating gastrulation movements. Development 2002, 129:2823-2834.
29. Joulia D., Bernardi H., Garandel V., Rabenoelina F., Vernus B., Cabello G. Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin. Exp. Cell Res. 2003, 286:263-275.
30. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
31. Lee J.D., Anderson K.V. Morphogenesis of the node and notochord: the cellular basis for the establishment and maintenance of left-right asymmetry in the mouse. Dev. Dyn. 2008.
32. Lee S.J., Reed L.A., Davies M.V., Girgenrath S., Goad M.E., Tomkinson K.N., Wright J.F., Barker C., Ehrmantraut G., Holmstrom J., Trowell B., Gertz B., Jiang M.S., Sebald S.M., Matzuk M., Li E., Liang L.F., Quattlebaum E., Stotish R.L., Wolfman N.M. Regulation of muscle growth by multiple ligands signaling through activin type II receptors. Proc. Natl Acad. Sci. USA 2005, 102:18117-18122.
33. Levin M. Left-right asymmetry in embryonic development: a comprehensive review. Mech. Dev. 2005, 122:3-25.
34. Liao W., Hong S.H., Chan B.H., Rudolph F.B., Clark S.C., Chan L. APOBEC-2, a cardiac- and skeletal muscle-specific member of the cytidine deaminase supergene family. Biochem. Biophys. Res. Commun. 1999, 260:398-404.
35. Liu F., Pouponnot C., Massague J. Dual role of the Smad4/DPC4 tumor suppressor in TGFbeta-inducible transcriptional complexes. Genes Dev. 1997, 11:3157-3167.
36. Marques S., Borges A.C., Silva A.C., Freitas S., Cordenonsi M., Belo J.A. The activity of the Nodal antagonist Cerl-2 in the mouse node is required for correct L/R body axis. Genes Dev. 2004, 18:2342-2347.
37. Massague J., Cheifetz S., Endo T., Nadal-Ginard B. Type beta transforming growth factor is an inhibitor of myogenic differentiation. Proc. Natl Acad. Sci. USA 1986, 83:8206-8210.
38. McMahon D.K., Anderson P.A., Nassar R., Bunting J.B., Saba Z., Oakeley A.E., Malouf N.N. C2C12 cells: biophysical, biochemical, and immunocytochemical properties. Am. J. Physiol. 1994, 266:C1795-C1802.
39. Mercola M. Left-right asymmetry: nodal points. J. Cell Sci. 2003, 116:3251-3257.
40. Mikl M.C., Watt I.N., Lu M., Reik W., Davies S.L., Neuberger M.S., Rada C. Mice deficient in APOBEC2 and APOBEC3. Mol. Cell. Biol. 2005, 25:7270-7277.
41. Navaratnam N., Sarwar R. An overview of cytidine deaminases. Int. J. Hematol. 2006, 83:195-200.
42. Ohi Y., Wright C.V. Anteriorward shifting of asymmetric Xnr1 expression and contralateral communication in left-right specification in Xenopus. Dev. Biol. 2007, 301:447-463.
43. Olson E.N., Sternberg E., Hu J.S., Spizz G., Wilcox C. Regulation of myogenic differentiation by type beta transforming growth factor. J. Cell Biol. 1986, 103:1799-1805.
44. Onuma Y., Yeo C.-Y., Whitman M. XCR2, one of three Xenopus EGF-CFC genes, has a distinct role in the regulation of left-right patterning. Development 2005, 133:237-250.
45. Pearce J.J., Penny G., Rossant J. A mouse cerberus/Dan-related gene family. Dev. Biol. 1999, 209:98-110.
46. Pfaffl M.W., Georgieva T.M., Georgiev I.P., Ontsouka E., Hageleit M., Blum J.W. Real-time RT-PCR quantification of insulin-like growth factor (IGF)-1, IGF-1 receptor, IGF-2, IGF-2 receptor, insulin receptor, growth hormone receptor, IGF-binding proteins 1, 2 and 3 in the bovine species. Domest. Anim. Endocrinol. 2002, 22:91-102.
47. 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.
48. Raya A., Belmonte J.C. Left-right asymmetry in the vertebrate embryo: from early information to higher-level integration. Nat. Rev. Genet. 2006, 7:283-293.
49. Rios R., Carneiro I., Arce V.M., Devesa J. Myostatin regulates cell survival during C2C12 myogenesis. Biochem. Biophys. Res. Commun. 2001, 280:561-566.
50. Rios R., Carneiro I., Arce V.M., Devesa J. Myostatin is an inhibitor of myogenic differentiation. Am. J. Physiol. Cell Physiol. 2002, 282:C993-C999.
51. Sato Y., Probst H.C., Tatsumi R., Ikeuchi Y., Neuberger M.S., Rada C. Deficiency in APOBEC2 leads to a shift in muscle fiber-type, diminished body mass and myopathy. J. Biol. Chem. 2009.
52. Schier A.F., Talbot W.S. Molecular genetics of axis formation in zebrafish. Annu. Rev. Genet. 2005, 39:561-613.
53. Schweickert A., Weber T., Beyer T., Vick P., Bogusch S., Feistel K., Blum M. Cilia-driven leftward flow determines laterality in Xenopus. Curr. Biol. 2007, 17:60-66.
54. Shiratori H., Hamada H. The left-right axis in the mouse: from origin to morphology. Development 2006, 133:2095-2104.
55. Shook D.R., Majer C., Keller R. Pattern and morphogenesis of presumptive superficial mesoderm in two closely related species, Xenopus laevis and Xenopus tropicalis. Dev. Biol. 2004, 270:163-185.
56. Smith H.C. RNA and DNA editing: molecular mechanisms and their integration into biological systems 2008, Wiley-Interscience, Hoboken, N.J.
57. Smith J.C. Mesoderm-inducing factors and mesodermal patterning. Curr. Opin. Cell Biol. 1995, 7:856-861.
58. Smith J.C., Price B.M., Green J.B., Weigel D., Herrmann B.G. Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 1991, 67:79-87.
59. Speder P., Petzoldt A., Suzanne M., Noselli S. Strategies to establish left/right asymmetry in vertebrates and invertebrates. Curr. Opin. Genet. Dev. 2007, 17:351-358.
60. Sun B.I., Bush S.M., Collins-Racie L.A., LaVallie E.R., DiBlasio-Smith E.A., Wolfman N.M., McCoy J.M., Sive H.L. Derriere: a TGF-beta family member required for posterior development in Xenopus. Development 1999, 126:1467-1482.
61. Tanaka C., Sakuma R., Nakamura T., Hamada H., Saijoh Y. Long-range action of Nodal requires interaction with GDF1. Genes Dev. 2007, 21:3272-3282.
62. Taylor M.F., Paulauskis J.D., Weller D.D., Kobzik L. In vitro efficacy of morpholino-modified antisense oligomers directed against tumor necrosis factor-alpha mRNA. J. Biol. Chem. 1996, 271:17445-17452.
63. Thisse B., Heyer V., Lux A., Alunni V., Degrave A., Seiliez I., Kirchner J., Parkhill J.P., Thisse C. Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Meth. Cell Biol. 2004, 77:505-519.
64. Thisse C., Thisse B., Schilling T.F., Postlethwait J.H. Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 1993, 119:1203-1215.
65. Vonica A., Brivanlou A.H. The left-right axis is regulated by the interplay of Coco, Xnr1 and derriere in Xenopus embryos. Dev. Biol. 2007, 303:281-294.
66. Vonica A., Gumbiner B.M. Zygotic Wnt activity is required for Brachyury expression in the early Xenopus laevis embryo. Dev. Biol. 2002, 250:112-127.
67. Whitman M. Nodal signaling in early vertebrate embryos: themes and variations. Dev. Cell 2001, 1:605-617.
68. Wilson P.A., Melton D.A. Mesodermal patterning by an inducer gradient depends on secondary cell-cell communication. Curr. Biol. 1994, 4:676-686.
69. Wrana J.L., Attisano L., Carcamo J., Zentella A., Doody J., Laiho M., Wang X.F., Massague J. TGF beta signals through a heteromeric protein kinase receptor complex. Cell 1992, 71:1003-1014.
70. Wright C.V. Mechanisms of left-right asymmetry: what's right and what's left?. Dev. Cell 2001, 1:179-186.
71. Yan Y.T., Liu J.J., Luo Y.E.C., Haltiwanger R.S., Abate-Shen C., Shen M.M. Dual roles of Cripto as a ligand and coreceptor in the nodal signaling pathway. Mol. Cell. Biol. 2002, 22:4439-4449.
72. Yelon D., Horne S.A., Stainier D.Y. Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. 1999, 214:23-37.
73. Yeo C., Whitman M. Nodal signals to Smads through Cripto-dependent and Cripto-independent mechanisms. Mol. Cell 2001, 7:949-957.