Bcl-wav and the mitochondrial calcium uniporter drive gastrula morphogenesis in zebrafish

Nature Communications

Volumn 4, Issue , 2013, Pages

  Prudent, Julien ^a   Popgeorgiev, Nikolay ^a   Bonneau, Benjamin ^a   Thibaut, Julien ^a   Gadet, Rudy ^a   Lopez, Jonathan ^a,b   Gonzalo, Philippe ^a,b   Rimokh, Ruth ^a   Manon, Stephen ^c   Houart, Corinne ^d   Herbomel, Philippe ^e   Aouacheria, Abdel ^f   Gillet, Germain ^a  

^a CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^b CROIX ROUSSE HOSPITAL   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e INSTITUT PASTEUR   (France)

^f UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BCL WAV PROTEIN; CALCIUM; HYBRID PROTEIN; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL; ZEBRAFISH PROTEIN;

APOPTOSIS; BIOCHEMISTRY; CALCIUM; CYPRINID; CYTOLOGY; EVOLUTIONARY BIOLOGY; FUNCTIONAL ROLE; METABOLISM; MITOCHONDRION; MOLECULAR ANALYSIS; MORPHOGENESIS; PROTEIN;

ANIMAL CELL; ARTICLE; BLASTOMA; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MIGRATION; CONTROLLED STUDY; GASTRULATION; MICROFILAMENT; MITOCHONDRIAL CALCIUM UNIPORTER; NONHUMAN; NOTOCHORD; ZEBRA FISH;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BIOLOGICAL TRANSPORT; BLASTOMERES; CALCIUM; CALCIUM CHANNELS; CELL MOVEMENT; CELLS, CULTURED; GASTRULA; GASTRULATION; GENE KNOCKDOWN TECHNIQUES; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MICE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MORPHOLINOS; NOTOCHORD; PROTO-ONCOGENE PROTEINS C-BCL-2; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; VOLTAGE-DEPENDENT ANION CHANNEL 1; ZEBRAFISH;

EID: 84883105440     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3330     Document Type: Article

References (44)

1. Youle, R. J. & Strasser, A. The BCL-2 protein family: opposing activities that mediate cell death. Nature reviews. Mol. Cell Biol. 9, 47-59 (2008).
2. Wang, C. & Youle, R. J. The role of mitochondria in apoptosis*. Annu. Rev. Genet. 43, 95-118 (2009).
3. Berridge, M. J., Bootman, M. D. & Roderick, H. L. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529 (2003). (Pubitemid 36773404)
4. Rizzuto, R. et al. Ca(2θ) transfer from the ER to mitochondria: when, how and why. Biochim. Biophys. Acta 1787, 1342-1351 (2009).
5. Rapizzi, E. et al. Recombinant expression of the voltage-dependent anion channel enhances the transfer of Ca2 θ microdomains to mitochondria. J. Cell Biol. 159, 613-624 (2002).
6. De Stefani, D., Raffaello, A., Teardo, E., Szabo, I. & Rizzuto, R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476, 336-340 (2011).
7. Baughman, J. M. et al. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476, 341-345 (2011).
8. Bonneau, B., Prudent, J., Popgeorgiev, N. & Gillet, G. Non-apoptotic roles of Bcl-2 family: the calcium connection. Biochim. Biophys. Acta 1833, 1755-1765 (2013).
9. Eimon, P. M. & Ashkenazi, A. The zebrafish as a model organism for the study of apoptosis. Apoptosis 15, 331-349 (2010).
10. Sepich, D. S., Usmani, M., Pawlicki, S. & Solnica-Krezel, L. Wnt/PCP signaling controls intracellular position of MTOCs during gastrulation convergence and extension movements. Development (Cambridge, England) 138, 543-552 (2011).
11. Kratz, E. et al. Functional characterization of the Bcl-2 gene family in the zebrafish. Cell Death Differ. 13, 1631-1640 (2006). (Pubitemid 44390851)
12. Webb, S. E. & Miller, A. L. Calcium signalling during embryonic development. Nat. Rev. Mol. Cell Biol. 4, 539-551 (2003). (Pubitemid 36773406)
13. Arnaud, E. et al. The zebrafish bcl-2 homologue Nrz controls development during somitogenesis and gastrulation via apoptosis-dependent and-independent mechanisms. Cell Death Differ. 13, 1128-1137 (2006). (Pubitemid 43905594)
14. Popgeorgiev, N. et al. The apoptotic regulator Nrz controls cytoskeletal dynamics via the regulation of Ca(2 θ) trafficking in the zebrafish blastula. Dev. Cell 20, 663-676 (2011).
15. Aouacheria, A., Rech de Laval, V., Deléage, G. & Combet, C. Characterization of the Bcl-2 family using structure-aided HMM Framework. JOBIM 79-80 (2010).
16. Kane, D. A. & Kimmel, C. B. The zebrafish midblastula transition. Development 119, 447-456 (1993). (Pubitemid 23293187)
17. Gerety, S. S. & Wilkinson, D. G. Morpholino artifacts provide pitfalls and reveal a novel role for pro-apoptotic genes in hindbrain boundary development. Dev. Biol. 350, 279-289 (2011).
18. Tan, W. & Colombini, M. VDAC closure increases calcium ion flux. Biochim. Biophys. Acta 1768, 2510-2515 (2007). (Pubitemid 47532032)
19. De Stefani, D. et al. VDAC1 selectively transfers apoptotic Ca2 θ signals to mitochondria. Cell Death Differ. 19, 267-273 (2012).
20. Roy, S. S. et al. Bad targets the permeability transition pore independent of Bax or Bak to switch between Ca2θ-dependent cell survival and death. Mol. Cell 33, 377-388 (2009).
21. Shimizu, S., Konishi, A., Kodama, T. & Tsujimoto, Y. BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc. Natl Acad. Sci. USA 97, 3100-3105 (2000). (Pubitemid 30183262)
22. Vander Heiden, M. G. et al. Bcl-xL promotes the open configuration of the voltage-dependent anion channel and metabolite passage through the outer mitochondrial membrane. J. Biol. Chem. 276, 19414-19419 (2001).
23. Vander Heiden, M. G., Chandel, N. S., Schumacker, P. T. & Thompson, C. B. Bcl-xL prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol. Cell 3, 159-167 (1999). (Pubitemid 29292617)
24. Wallingford, J. B., Ewald, A. J., Harland, R. M. & Fraser, S. E. Calcium signaling during convergent extension in Xenopus. Curr. Biol. 11, 652-661 (2001). (Pubitemid 32418161)
25. Markova, O. & Lenne, P. F. Calcium signaling in developing embryos: Focus on the regulation of cell shape changes and collective movements. Semin. Cell Dev. Biol. 23, 298-307 (2012).
26. Gilland, E., Miller, A. L., Karplus, E., Baker, R. & Webb, S. E. Imaging of multicellular large-scale rhythmic calcium waves during zebrafish gastrulation. Proc. Natl Acad. Sci. USA 96, 157-161 (1999). (Pubitemid 29036069)
27. Freisinger, C. M., Fisher, R. A. & Slusarski, D. C. Regulator of g protein signaling 3 modulates wnt5b calcium dynamics and somite patterning. PLoS Genet. 6, 1001020 (2010).
28. Guillemin, Y. et al. Oocytes and early embryos selectively express the survival factor BCL2L10. J. Mol. Med. 87, 923-940 (2009).
29. Guillemin, Y., Cornut-Thibaut, A., Gillet, G., Penin, F. & Aouacheria, A. Characterization of unique signature sequences in the divergent maternal protein Bcl2l10. Mol. Biol. Evol. 28, 3271-3283 (2011).
30. Rinkenberger, J. L., Horning, S., Klocke, B., Roth, K. & Korsmeyer, S. J. Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev. 14, 23-27 (2000). (Pubitemid 30051575)
31. Aouacheria, A., Brunet, F. & Gouy, M. Phylogenomics of life-or-death switches in multicellular animals: Bcl-2, BH3-Only, and BNip families of apoptotic regulators. Mol. Biol. Evol. 22, 2395-2416 (2005). (Pubitemid 41662342)
32. Roy, S. S., Ehrlich, A. M., Craigen, W. J. & Hajnoczky, G. VDAC2 is required for truncated BID-induced mitochondrial apoptosis by recruiting BAK to the mitochondria. EMBO Rep. 10, 1341-1347 (2009).
33. Tsujimoto, Y. & Shimizu, S. VDAC regulation by the Bcl-2 family of proteins. Cell Death Differ. 7, 1174-1181 (2000). (Pubitemid 32042224)
34. Tada, M., Concha, M. L. & Heisenberg, C. P. Non-canonical Wnt signalling and regulation of gastrulation movements. Semin. Cell Dev. Biol. 13, 251-260 (2002). (Pubitemid 35304530)
35. Zhu, S., Liu, L., Korzh, V., Gong, Z. & Low, B. C. RhoA acts downstream of Wnt5 and Wnt11 to regulate convergence and extension movements by involving effectors Rho kinase and diaphanous: use of zebrafish as an in vivo model for GTPase signaling. Cell Signal 18, 359-372 (2006). (Pubitemid 41661351)
36. Kardash, E. et al. A role for Rho GTPases and cell-cell adhesion in single-cell motility in vivo. Nat. Cell Biol. 12, 47-53 (2010).
37. Sheldahl, L. C. et al. Dishevelled activates Ca2 θ flux, PKC, and CamKII in vertebrate embryos. J. Cell Biol. 161, 769-777 (2003). (Pubitemid 36648760)
38. Kohn, A. D. & Moon, R. T. Wnt and calcium signaling: beta-catenin-independent pathways. Cell Calcium 38, 439-446 (2005). (Pubitemid 41283282)
39. Webb, S. E. & Miller, A. L. Ca2 θ signalling and early embryonic patterning during zebrafish development. Clin. Exp. Pharmacol. Physiol. 34, 897-904 (2007). (Pubitemid 47083975)
40. Yin, C. & Solnica-Krezel, L. Convergence and extension movements mediate the specification and fate maintenance of zebrafish slow muscle precursors. Dev. Biol. 304, 141-155 (2007). (Pubitemid 46399686)
41. Moradi-Ameli, M., Lorca, T., Ficheux, D., di Pietro, A. & Gillet, G. Interaction between the antiapoptotic protein Nr-13 and cytochrome c. Antagonistic effect of the BH3 domain of Bax. Biochemistry 41, 8540-8550 (2002). (Pubitemid 34743293)
42. Gillet, G., Guerin, M., Trembleau, A. & Brun, G. A Bcl-2-related gene is activated in avian cells transformed by the Rous sarcoma virus. EMBO J. 14, 1372-1381 (1995).
43. Thisse, C. & Thisse, B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 3, 59-69 (2008).
44. Koppen, M., Fernandez, B. G., Carvalho, L., Jacinto, A. & Heisenberg, C. P. Coordinated cell-shape changes control epithelial movement in zebrafish and Drosophila. Development (Cambridge, England) 133, 2671-2681 (2006). (Pubitemid 44177888).