Connexin26-mediated transfer of laterality cues in Xenopus

Biology Open

Volumn 1, Issue 5, 2012, Pages 473-481

  Beyer, Tina ^a   Thumberger, Thomas ^a,b   Schweickert, Axel ^a   Blum, Martin ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Connexin; Cx26; Cx32; Gap junctional communication; Gap junctions; Left right asymmetry; Xenopus laevis

Indexed keywords

EID: 84964865489     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.2012760     Document Type: Article

References (76)

1. Ayad, W. A., Locke, D., Koreen, I. V. and Harris, A. L. (2006). Heteromeric, but not homomeric, connexin channels are selectively permeable to inositol phosphates. J. Biol. Chem. 281, 16727-16739.
2. Barrio, L. C., Suchyna, T., Bargiello, T., Xu, L. X., Roginski, R. S., Bennett, M. V. and Nicholson, B. J. (1991). Gap junctions formed by connexins 26 and 32 alone and in combination are differently affected by applied voltage. Proc. Natl. Acad. Sci. USA 88, 8410-8414.
3. Belo, J. A., Bouwmeester, T., Leyns, L., Kertesz, N., Gallo, M., Follettie, M. and De Robertis, E. M. (1997). Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech. Dev. 68, 45-57.
4. Bevans, C. G., Kordel, M., Rhee, S. K. and Harris, A. L. (1998). Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules. J. Biol. Chem. 273, 2808-2816.
5. Beyer, T., Danilchik, M., Thumberger, T., Vick, P., Tisler, M., Schneider, I., Bogusch, S., Andre, P., Ulmer, B., Walentek, P. et al. (2012). Serotonin signaling is required for Wnt-dependent GRP specification and leftward flow in Xenopus. Curr. Biol. 22, 33-39.
6. Blum, M., Andre, P., Muders, K., Schweickert, A., Fischer, A., Bitzer, E., Bogusch, S., Beyer, T., van Straaten, H. W. M. and Viebahn, C. (2007). Ciliation and gene expression distinguish between node and posterior notochord in the mammalian embryo. Differentiation 75, 133-146.
7. Blum, M., Weber, T., Beyer, T. and Vick, P. (2009). Evolution of leftward flow. Semin. Cell Dev. Biol. 20, 464-471.
8. Britz-Cunningham, S. H., Shah, M. M., Zuppan, C. W. and Fletcher, W. H. (1995). Mutations of the Connexin43 gap-junction gene in patients with heart malformations and defects of laterality. N. Engl. J. Med. 332, 1323-1329.
9. Burn, S. F. and Hill, R. E. (2009). Left-right asymmetry in gut development: what happens next? Bioessays 31, 1026-1037.
10. Capdevila, J., Vogan, K. J., Tabin, C. J. and Izpisúa Belmonte, J. C. (2000). Mechanisms of left-right determination in vertebrates. Cell 101, 9-21.
11. Casey, B. and Ballabio, A. (1995). Connexin43 mutations in sporadic and familial defects of laterality. N. Engl. J. Med. 333, 941-942 [Letter to Editor].
12. Cotrina, M. L., Lin, J. H., Alves-Rodrigues, A., Liu, S., Li, J., Azmi-Ghadimi, H., Kang, J., Naus, C. C. and Nedergaard, M. (1998). Connexins regulate calcium signaling by controlling ATP release. Proc. Natl. Acad. Sci. USA 95, 15735-15740.
13. Cotrina, M. L., Lin, J. H., López-García, J. C., Naus, C. C. and Nedergaard, M. (2000). ATP-mediated glia signaling. J. Neurosci. 20, 2835-2844.
14. De Boer, T. P., Kok, B., Neuteboom, K. I. E., Spieker, N., De Graaf, J., Destrée, O. H. J., Rook, M. B., Van Veen, T. A. B., Jongsma, H. J., Vos, M. A. et al. (2005). Cloning and functional characterization of a novel connexin expressed in somites of Xenopus laevis. Dev. Dyn. 233, 864-871.
15. de Boer, T. P., Kok, B., Roël, G., van Veen, T. A. B., Destrée, O. H. J., Rook, M. B., Vos, M. A., de Bakker, J. M. T. and van der Heyden, M. A. G. (2006). Cloning, embryonic expression, and functional characterization of two novel connexins from Xenopus laevis. Biochem. Biophys. Res. Commun. 349, 855-862.
16. Debrus, S., Tuffery, S., Matsuoka, R., Galal, O., Sarda, P., Sauer, U., Bozio, A., Tanman, B., Toutain, A., Claustres, M. et al. (1997). Lack of evidence for connexin 43 gene mutations in human autosomal recessive lateralization defects. J. Mol. Cell. Cardiol. 29, 1423-1431.
17. Feistel, K. and Blum, M. (2008). Gap junctions relay FGF8-mediated right-sided repression of Nodal in rabbit. Dev. Dyn. 237, 3516-3527.
18. Field, S., Riley, K.-L., Grimes, D. T., Hilton, H., Simon, M., Powles-Glover, N., Siggers, P., Bogani, D., Greenfield, A. and Norris, D. P. (2011). Pkd1l1 establishes left-right asymmetry and physically interacts with Pkd2. Development 138, 1131-1142.
19. Finkbeiner, S. (1992). Calcium waves in astrocytes-filling in the gaps. Neuron 8, 1101-1108.
20. Fukumoto, T., Kema, I. P. and Levin, M. (2005). Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Curr. Biol. 15, 794-803.
21. Gabriel, H. D., Jung, D., Bützler, C., Temme, A., Traub, O., Winterhager, E. and Willecke, K. (1998). Transplacental uptake of glucose is decreased in embryonic lethal connexin26-deficient mice. J. Cell Biol. 140, 1453-1461.
22. Gebbia, M., Towbin, J. A. and Casey, B. (1996). Failure to detect connexin43 mutations in 38 cases of sporadic and familial heterotaxy. Circulation 94, 1909-1912.
23. Goodenough, D. A. and Paul, D. L. (2003). Beyond the gap: functions of unpaired connexon channels. Nat. Rev. Mol. Cell Biol. 4, 285-295.
24. Gros, J., Feistel, K., Viebahn, C., Blum, M. and Tabin, C. J. (2009). Cell movements at Hensen's node establish left/right asymmetric gene expression in the chick. Science 324, 941-944.
25. Guan, X., Cravatt, B. F., Ehring, G. R., Hall, J. E., Boger, D. L., Lerner, R. A. and Gilula, N. B. (1997). The sleep-inducing lipid oleamide deconvolutes gap junction communication and calcium wave transmission in glial cells. J. Cell Biol. 139, 1785-1792.
26. Guthrie, P. B., Knappenberger, J., Segal, M., Bennett, M. V., Charles, A. C. and Kater, S. B. (1999). ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19, 520-528.
27. Hamada, H. (2008). Breakthroughs and future challenges in left-right patterning. Dev. Growth Differ. 50 Suppl 1:, S71-S78.
28. Hamada, H., Meno, C., Watanabe, D. and Saijoh, Y. (2002). Establishment of vertebrate left-right asymmetry. Nat. Rev. Genet. 3, 103-113.
29. Hatler, J. M., Essner, J. J. and Johnson, R. G. (2009). A gap junction connexin is required in the vertebrate left-right organizer. Dev. Biol. 336, 183-191.
30. Hirokawa, N., Tanaka, Y., Okada, Y. and Takeda, S. (2006). Nodal flow and the generation of left-right asymmetry. Cell 125, 33-45.
31. Hojo, M., Takashima, S., Kobayashi, D., Sumeragi, A., Shimada, A., Tsukahara, T., Yokoi, H., Narita, T., Jindo, T., Kage, T. et al. (2007). Right-elevated expression of charon is regulated by fluid flow in medaka Kupffer's vesicle. Dev. Growth Differ. 49, 395-405.
32. Juszczak, G. R. and Swiergiel, A. H. (2009). Properties of gap junction blockers and their behavioural, cognitive and electrophysiological effects: animal and human studies. Prog. Neuropsychopharmacol. Biol. Psychiatry 33, 181-198.
33. Jørgensen, N. R., Henriksen, Z., Sørensen, O. H., Eriksen, E. F., Civitelli, R. and Steinberg, T. H. (2002). Intercellular calcium signaling occurs between human osteoblasts and osteoclasts and requires activation of osteoclast P2X7 receptors. J. Biol. Chem. 277, 7574-7580.
34. Kamura, K., Kobayashi, D., Uehara, Y., Koshida, S., Iijima, N., Kudo, A., Yokoyama, T. and Takeda, H. (2011). Pkd1l1 complexes with Pkd2 on motile cilia and functions to establish the left-right axis. Development 138, 1121-1129.
35. Kunimoto, K., Yamazaki, Y., Nishida, T., Shinohara, K., Ishikawa, H., Hasegawa, T., Okanoue, T., Hamada, H., Noda, T., Tamura, A. et al. (2012). Coordinated ciliary beating requires Odf2-mediated polarization of basal bodies via basal feet. Cell 148, 189-200.
36. Landesman, Y., Goodenough, D. A. and Paul, D. L. (2000). Gap junctional communication in the early Xenopus embryo. J. Cell Biol. 150, 929-936.
37. Landesman, Y., Postma, F. R., Goodenough, D. A. and Paul, D. L. (2003). Multiple connexins contribute to intercellular communication in the Xenopus embryo. J. Cell Sci. 116, 29-38.
38. Lee, J. D. and Anderson, K. V. (2008). Morphogenesis of the node and notochord: the cellular basis for the establishment and maintenance of left-right asymmetry in the mouse. Dev. Dyn. 237, 3464-3476.
39. Levin, M. (2005). Left-right asymmetry in embryonic development: a comprehensive review. Mech. Dev. 122, 3-25.
40. Levin, M. (2007). Gap junctional communication in morphogenesis. Prog. Biophys. Mol. Biol. 94, 186-206.
41. Levin, M. and Mercola, M. (1998). Gap junctions are involved in the early generation of left-right asymmetry. Dev. Biol. 203, 90-105.
42. Levin, M. and Mercola, M. (1999). Gap junction-mediated transfer of left-right patterning signals in the early chick blastoderm is upstream of Shh asymmetry in the node. Development 126, 4703-4714.
43. Levin, M., Thorlin, T., Robinson, K. R., Nogi, T. and Mercola, M. (2002). Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111, 77-89.
44. Maisonneuve, C., Guilleret, I., Vick, P., Weber, T., Andre, P., Beyer, T., Blum, M. and Constam, D. B. (2009). Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow. Development 136, 3019-3030.
45. Marjoram, L. and Wright, C. (2011). Rapid differential transport of Nodal and Lefty on sulfated proteoglycan-rich extracellular matrix regulates left-right asymmetry in Xenopus. Development 138, 475-485.
46. Männer, J. (2009). The anatomy of cardiac looping: a step towards the understanding of the morphogenesis of several forms of congenital cardiac malformations. Clin. Anat. 22, 21-35.
47. McGrath, J., Somlo, S., Makova, S., Tian, X. and Brueckner, M. (2003). Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114, 61-73.
48. Nelles, E., Bützler, C., Jung, D., Temme, A., Gabriel, H. D., Dahl, U., Traub, O., Stümpel, F., Jungermann, K., Zielasek, J. et al. (1996). Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc. Natl. Acad. Sci. USA 93, 9565-9570.
49. Oki, S., Hashimoto, R., Okui, Y., Shen, M. M., Mekada, E., Otani, H., Saijoh, Y. and Hamada, H. (2007). Sulfated glycosaminoglycans are necessary for Nodal signal transmission from the node to the left lateral plate in the mouse embryo. Development 134, 3893-3904.
50. Oki, S., Kitajima, K., Marques, S., Belo, J. A., Yokoyama, T., Hamada, H. and Meno, C. (2009). Reversal of left-right asymmetry induced by aberrant Nodal signaling in the node of mouse embryos. Development 136, 3917-3925.
51. Paul, D. L., Yu, K., Bruzzone, R., Gimlich, R. L. and Goodenough, D. A. (1995). Expression of a dominant negative inhibitor of intercellular communication in the early Xenopus embryo causes delamination and extrusion of cells. Development 121, 371-381.
52. Pennekamp, P., Karcher, C., Fischer, A., Schweickert, A., Skryabin, B., Horst, J., Blum, M. and Dworniczak, B. (2002). The ion channel polycystin-2 is required for left-right axis determination in mice. Curr. Biol. 12, 938-943.
53. Sarmah, B., Latimer, A. J., Appel, B. and Wente, S. R. (2005). Inositol polyphosphates regulate zebrafish left-right asymmetry. Dev. Cell 9, 133-145.
54. Scherer, S. S., Xu, Y. T., Nelles, E., Fischbeck, K., Willecke, K. and Bone, L. J. (1998). Connexin32-null mice develop demyelinating peripheral neuropathy. Glia 24, 8-20.
55. Schier, A. F. (2003). Nodal signaling in vertebrate development. Annu. Rev. Cell Dev. Biol. 19, 589-621.
56. Schweickert, A., Weber, T., Beyer, T., Vick, P., Bogusch, S., Feistel, K. and Blum, M. (2007). Cilia-driven leftward flow determines laterality in Xenopus. Curr. Biol. 17, 60-66.
57. Schweickert, A., Vick, P., Getwan, M., Weber, T., Schneider, I., Eberhardt, M., Beyer, T., Pachur, A. and Blum, M. (2010). The nodal inhibitor Coco is a critical target of leftward flow in Xenopus. Curr. Biol. 20, 738-743.
58. Schweickert, A., Walentek, P., Thumberger, T. and Danilchik, M. (2012). Linking early determinants and cilia-driven leftward flow in left-right axis specification of Xenopus laevis: A theoretical approach. Differentiation 83, S67-S77.
59. Shen, M. M. (2007). Nodal signaling: developmental roles and regulation. Development 134, 1023-1034.
60. Shook, D. R., Majer, C. and Keller, R. (2004). Pattern and morphogenesis of presumptive superficial mesoderm in two closely related species, Xenopus laevis and Xenopus tropicalis. Dev. Biol. 270, 163-185.
61. Slusarski, D. C. and Pelegri, F. (2007). Calcium signaling in vertebrate embryonic patterning and morphogenesis. Dev. Biol. 307, 1-13.
62. Sosinsky, G. (1995). Mixing of connexins in gap junction membrane channels. Proc. Natl. Acad. Sci. USA 92, 9210-9214.
63. Splitt, M. P., Burn, J. and Goodship, J. (1995). Connexin43 mutations in sporadic and familial defects of laterality. N. Engl. J. Med. 333, 941-942 [Letter to Editor].
64. Stout, C., Goodenough, D. A. and Paul, D. L. (2004). Connexins: functions without junctions. Curr. Opin. Cell Biol. 16, 507-512.
65. Sulik, K., Dehart, D. B., Inagaki, T., Carson, J. L., Vrablic, T., Gesteland, K. and Schoenwolf, G. C. (1994). Morphogenesis of the murine node and notochordal plate. Dev. Dyn. 201, 260-278.
66. Tabin, C. (2005). Do we know anything about how left-right asymmetry is first established in the vertebrate embryo? J. Mol. Histol. 36, 317-323.
67. van der Heyden, M. A., Roeleveld, L., Peterson, J. and Destrée, O. H. (2001). Connexin43 expression during Xenopus development. Mech. Dev. 108, 217-220.
68. Vandenberg, L. N. and Levin, M. (2009). Perspectives and open problems in the early phases of left-right patterning. Semin. Cell Dev. Biol. 20, 456-463.
69. Vandenberg, L. N. and Levin, M. (2010). Far from solved: a perspective on what we know about early mechanisms of left-right asymmetry. Dev. Dyn. 239, 3131-3146.
70. Vick, P., Schweickert, A., Weber, T., Eberhardt, M., Mencl, S., Shcherbakov, D., Beyer, T. and Blum, M. (2009). Flow on the right side of the gastrocoel roof plate is dispensable for symmetry breakage in the frog Xenopus laevis. Dev. Biol. 331, 281-291.
71. Viotti, M., Niu, L., Shi, S.-H. and Hadjantonakis, A.-K. (2012). Role of the gut endoderm in relaying left-right patterning in mice. PLoS Biol. (in press).
72. Walentek, P., Beyer, T., Thumberger, T., Schweickert, A. and Blum, M. (2012). ATP4a is required for Wnt-dependent Foxj1 expression and leftward flow in Xenopus left-right development. Cell Rep. (in press).
73. Wann, A. K. T., Zuo, N., Haycraft, C. J., Jensen, C. G., Poole, C. A., McGlashan, S. R. and Knight, M. M. (2012). Primary cilia mediate mechanotransduction through control of ATP-induced Ca2+ signaling in compressed chondrocytes. FASEB J. [Epub ahead of print].
74. Ye, Z.-C., Wyeth, M. S., Baltan-Tekkok, S. and Ransom, B. R. (2003). Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J. Neurosci. 23, 3588-3596.
75. Yelin, R., Schyr, R. B.-H., Kot, H., Zins, S., Frumkin, A., Pillemer, G. and Fainsod, A. (2005). Ethanol exposure affects gene expression in the embryonic organizer and reduces retinoic acid levels. Dev. Biol. 279, 193-204.
76. Yelin, R., Kot, H., Yelin, D. and Fainsod, A. (2007). Early molecular effects of ethanol during vertebrate embryogenesis. Differentiation 75, 393-403.