Cell organization, growth, and neural and cardiac development require αII-spectrin

Journal of Cell Science

Volumn 124, Issue 23, 2011, Pages 3956-3966

  Stankewich, Michael C ^a   Cianci, Carol D ^a   Stabach, Paul R ^a   Ji, Lan ^a   Nath, Anjali ^a   Morrow, Jon S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin cytoskeleton; Ankyrin; Axons; Cell growth; Development; Exon trap; Myocardium; Neuroepithelial cell; Ventricular zone

Indexed keywords

ACTIN; ANKYRIN; CELL PROTEIN; FIBRONECTIN; SPECTRIN; SPECTRIN ALPHA2; SPECTRIN BETA; SPECTRIN BETA1; SPECTRIN BETA2; SPECTRIN BETA3; SPNA2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; CELL GROWTH; CELL MIGRATION; CELL SHAPE; CELL SPREADING; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM CELL; ERYTHROCYTE; FEMALE; FIBROBLAST; GENE DELETION; HEART DEVELOPMENT; INTRAUTERINE GROWTH RETARDATION; LAMELLIPODIUM; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL TUBE DEFECT; NEUROEPITHELIUM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEPLETION; PROTEIN EXPRESSION;

ACTINS; ANIMALS; ANKYRINS; AXONS; BODY PATTERNING; CARRIER PROTEINS; CELL MEMBRANE; CELL POLARITY; CELL PROLIFERATION; CRANIOFACIAL ABNORMALITIES; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; FIBROBLASTS; GENE DELETION; HEART DEFECTS, CONGENITAL; MALE; MICE; MICE, INBRED C57BL; MICROFILAMENT PROTEINS; NEURAL TUBE DEFECTS; NEUROEPITHELIAL CELLS; PHENOTYPE; PROTEIN STABILITY; PSEUDOPODIA; SPECTRIN;

ANIMALIA; MUS; VERTEBRATA;

EID: 84856855005     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.080374     Document Type: Article

References (61)

1. Bellenchi, G. C., Gurniak, C. B., Perlas, E., Middei, S., Ammassari-Teule, M. and Witke, W. (2007). N-cofilin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex. Genes. Dev. 21, 2347-2357.
2. Bennett, V. and Baines, A. J. (2001). Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81, 1353-1392.
3. Bennett, V. and Healy, J. (2008). Organizing the fluid membrane bilayer: diseases linked to spectrin and ankyrin. Trends Mol. Med. 14, 28-36.
4. Bialkowska, K., Saido, T. C. and Fox, J. E. (2005). SH3 domain of spectrin participates in the activation of Rac in specialized calpain-induced integrin signaling complexes. J. Cell Sci. 118, 381-395.
5. Bloch, R. J. and Morrow, J. S. (1989). An unusual b-spectrin associated with clustered acetylcholine receptors. J. Cell Biol. 108, 481-493.
6. Bournier, O., Kroviarski, Y., Rotter, B., Nicolas, G., Lecomte, M. C. and Dhermy, D. (2006). Spectrin interacts with EVL (Enabled/vasodilator-stimulated phosphoprotein-like protein), a protein involved in actin polymerization. Biol. Cell. 98, 279-293.
7. Chan, W., Kordeli, E. and Bennett, V. (1993). 440-kD ankyrinB: structure of the major developmentally regulated domain and selective localization in unmyelinated axons. J. Cell Biol. 123, 1463-1473.
8. Cianci, C. D., Giorgi, M. and Morrow, J. S. (1988). Phosphorylation of ankyrin downregulates its cooperative interaction with spectrin and protein 3. J. Cell Biochem. 37, 301-315.
9. Clarkson, Y. L., Gillespie, T., Perkins, E. M., Lyndon, A. R. and Jackson, M. (2010). {beta}-III spectrin mutation L253P associated with spinocerebellar ataxia type 5 interferes with binding to Arp1 and protein trafficking from the Golgi. Hum. Mol. Genet. 19, 3634-3641.
10. De Matteis, M. A. and Morrow, J. S. (2000). Spectrin tethers and mesh in the biosynthetic pathway. J. Cell Sci. 113, 2331-2343.
11. Dubreuil, R. R. (2006). Functional links between membrane transport and the spectrin cytoskeleton. J. Membr. Biol. 211, 151-161.
12. Eigenthaler, M., Engelhardt, S., Schinke, B., Kobsar, A., Schmitteckert, E., Gambaryan, S., Engelhardt, C. M., Krenn, V., Eliava, M., Jarchau, T. et al. (2003). Disruption of cardiac Ena-VASP protein localization in intercalated disks causes dilated cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol. 285, H2471-H2481.
13. Gallagher, P. G. and Jarolim, P. (2000). red cell membrane disorders. In Hematology: Basic Principles and Practice, 5th edn (eds R. Hoffman, E. J. Benz, Jr, S. J. Shattil, B. Furie, H. J. Cohen, L. E. Silberstein and P. McGlave), pp. 576-610. New York: Churchill Livingstone.
14. Garbe, D. S., Das, A., Dubreuil, R. R. and Bashaw, G. J. (2007). beta-Spectrin functions independently of Ankyrin to regulate the establishment and maintenance of axon connections in the Drosophila embryonic CNS. Development 134, 273-284.
15. Golestaneh, N., Tang, Y., Katuri, V., Jogunoori, W., Mishra, L. and Mishra, B. (2006). Cell cycle deregulation and loss of stem cell phenotype in the subventricular zone of TGF-beta adaptor elf-/- mouse brain. Brain Res. 1108, 45-53.
16. Gotz, M. and Huttner, W. B. (2005). The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788.
17. Hammarlund, M., Jorgensen, E. M. and Bastiani, M. J. (2007). Axons break in animals lacking beta-spectrin. J. Cell Biol. 176, 269-275.
18. Hanspal, M. and Palek, J. (1987). Synthesis and assembly of membrane skeletal proteins in mammalian red cell precursors. J. Cell Biol. 105, 1417-1424.
19. Harris, A. S. and Morrow, J. S. (1990). Calmodulin and calcium-dependent protease I coordinately regulate the interaction of fodrin with actin. Proc. Natl. Acad. Sci USA 87, 3009-3013.
20. Harris, A. S., Green, L. A., Ainger, K. J. and Morrow, J. S. (1985). Mechanism of cytoskeletal regulation (I): functional differences correlate with antigenic dissimilarity in human brain and erythrocyte spectrin. Biochim. Biophys. Acta 830, 147-158.
21. Holleran, E. A., Ligon, L. A., Tokito, M., Stankewich, M. C., Morrow, J. S. and Holzbaur, E. L. (2001). beta III spectrin binds to the Arp1 subunit of dynactin. J. Biol. Chem. 276, 36598-36605.
22. Hulsmeier, J., Pielage, J., Rickert, C., Technau, G. M., Klambt, C. and Stork, T. (2007). Distinct functions of alpha-Spectrin and beta-Spectrin during axonal pathfinding. Development 134, 713-722.
23. Ikeda, Y., Dick, K. A., Weatherspoon, M. R., Gincel, D., Armbrust, K. R., Dalton, J. C., Stevanin, G., Durr, A., Zuhlke, C., Burk, K. et al. (2006). Spectrin mutations cause spinocerebellar ataxia type 5. Nat. Genet. 38, 184-190.
24. Kizhatil, K., Yoon, W., Mohler, P. J., Davis, L. H., Hoffman, J. A. and Bennett, V. (2007). Ankyrin-G and beta2-spectrin collaborate in biogenesis of lateral membrane of human bronchial epithelial cells. J. Biol. Chem. 282, 2029-2037.
25. Kordeli, E., Lambert, S. and Bennett, V. (1995). AnkyrinG. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J. Biol. Chem. 270, 2352-2359.
26. Lecomte, M. C., Nicolas, G., Fournier, C., Galand, C., Malbert-Colas, L., Bournier, O., Dhermy, D. and Grandchamps, B. (2001). Interaction of spectrin with the low molecular weight phosphotyrosine phosphatese (LMW-PTP). Cell Mol. Biol. Lett. 6, 216.
27. Li, D., Tang, H. Y. and Speicher, D. W. (2008). A structural model of the erythrocyte spectrin heterodimer initiation site determined using homology modeling and chemical cross-linking. J. Biol. Chem. 283, 1553-1562.
28. Luo, L. and O'Leary, D. D. (2005). Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28, 127-156.
29. Mangeat, P. H. and Burridge, K. (1984). Immunoprecipitation of nonerythrocyte spectrin within live cells following microinjection of specific antibodies: relation to cytoskeletal structures. J. Cell Biol. 98, 1363-1377.
30. McMahon, L. W., Walsh, C. E. and Lambert, M. W. (1999). Human alpha spectrin II and the fanconi anemia proteins FANCA and FANCC interact to form a nuclear complex. J. Biol. Chem. 274, 32904-32908.
31. Metral, S., Machnicka, B., Bigot, S., Colin, Y., Dhermy, D. and Lecomte, M. C. (2009). AlphaII-spectrin is critical for cell adhesion and cell cycle. J. Biol. Chem. 284, 2409-2418.
32. Mishra, L., Cai, T., Yu, P., Monga, S. P. and Mishra, B. (1999). Elf3 encodes a novel 200-kD beta-spectrin: role in liver development. Oncogene 18, 353-364.
33. Moorthy, S., Chen, L. and Bennett, V. (2000). Caenorhabditis elegans beta-G spectrin is dispensable for establishment of epithelial polarity, but essential for muscular and neuronal function. J. Cell Biol. 149, 915-930.
34. Muresan, V., Stankewich, M. C., Steffen, W., Morrow, J. S., Holzbaur, E. L. and Schnapp, B. J. (2001). Dynactin-dependent, dynein-driven vesicle transport in the absence of membrane proteins: a role for spectrin and acidic phospholipids. Mol. Cell 7, 173-183.
35. Nedrelow, J. H., Cianci, C. D. and Morrow, J. S. (2003). c-Src binds alpha II spectrin's Src homology 3 (SH3) domain and blocks calpain susceptibility by phosphorylating Tyr1176. J. Biol. Chem. 278, 7735-7741.
36. Nicolas, G., Fournier, C. M., Galand, C., Malbert-Colas, L., Bournier, O., Kroviarski, Y., Bourgeois, M., Camonis, J. H., Dhermy, D., Grandchamp, B. et al. (2002). Tyrosine phosphorylation regulates alpha II spectrin cleavage by calpain. Mol. Cell Biol. 22, 3527-3536.
37. Perkins, E. M., Clarkson, Y. L., Sabatier, N., Longhurst, D. M., Millward, C. P., Jack, J., Toraiwa, J., Watanabe, M., Rothstein, J. D., Lyndon, A. R. et al. (2010). Loss of beta-III spectrin leads to Purkinje cell dysfunction recapitulating the behavior and neuropathology of spinocerebellar ataxia type 5 in humans. J. Neurosci. 30, 4857-4867.
38. Pradhan, D. and Morrow, J. (2002). The spectrin-ankyrin skeleton controls CD45 surface display and interleukin-2 production. Immunity 17, 303-315.
39. Pumplin, D. W. (1995). The membrane skeleton of acetylcholine receptor domains in rat myotubes contains antiparallel homodimers of β-spectrin in filaments quantitatively resembling those of erythrocytes. J. Cell Sci. 108, 3145-3154.
40. Qi, X., Yang, G., Yang, L., Lan, Y., Weng, T., Wang, J., Wu, Z., Xu, J., Gao, X. and Yang, X. (2007). Essential role of Smad4 in maintaining cardiomyocyte proliferation during murine embryonic heart development. Dev. Biol. 311, 136-146.
41. Ramser, E. M., Buck, F., Schachner, M. and Tilling, T. (2010). Binding of alphaII spectrin to 14-3-3beta is involved in NCAM-dependent neurite outgrowth. Mol. Cell Neurosci. 45, 66-74.
42. Sato, M. and Nagano, T. (2005). Involvement of filamin A and filamin A-interacting protein (FILIP) in controlling the start and cell shape of radially migrating cortical neurons. Anat. Sci. Int. 80, 19-29.
43. Stabach, P. R., Devarajan, P., Stankewich, M. C., Bannykh, S. and Morrow, J. S. (2008). Ankyrin facilitates intracellular trafficking of alpha1-Na+-K+-ATPase in polarized cells. Am. J. Physiol. Cell Physiol. 295, C1202-C1214.
44. Stabach, P. R., Simonovic, I., Ranieri, M. A., Aboodi, M. S., Steitz, T. A., Simonovic, M. and Morrow, J. S. (2009). The structure of the ankyrin-binding site of betaspectrin reveals how tandem spectrin-repeats generate unique ligand-binding properties. Blood 113, 5377-5384.
45. Stankewich, M. C., Stabach, P. R. and Morrow, J. S. (2006). Human Sec31B: a family of new mammalian orthologues of yeast Sec31p that associate with the COPII coat. J. Cell Sci. 119, 958-969.
46. Stankewich, M. C., Gwynn, B., Ardito, T., Ji, L., Kim, J., Robledo, R. F., Lux, S. E., Peters, L. L. and Morrow, J. S. (2010). Targeted deletion of betaIII spectrin impairs synaptogenesis and generates ataxic and seizure phenotypes. Proc. Natl. Acad. Sci. USA 107, 6022-6027.
47. Stankewich, M. C., Tse, W. T., Peters, L. L., Ch'ng, Y., John, K. M., Stabach, P. R., Devarajan, P., Morrow, J. S. and Lux, S. E. (1998). A widely expressed betaIII spectrin associated with Golgi and cytoplasmic vesicles. Proc. Natl. Acad. Sci. USA 95, 14158-14163.
48. Street, M., Marsh, S. J., Stabach, P. R., Morrow, J. S., Brown, D. A. and Buckley, N. J. (2006). Stimulation of Galphaq-coupled M1 muscarinic receptor causes reversible spectrin redistribution mediated by PLC, PKC and ROCK. J. Cell Sci. 119, 1528-1536.
49. Tahirovic, S., Hellal, F., Neukirchen, D., Hindges, R., Garvalov, B. K., Flynn, K. C., Stradal, T. E., Chrostek-Grashoff, A., Brakebusch, C. and Bradke, F. (2010). Rac1 regulates neuronal polarization through the WAVE complex. J. Neurosci. 30, 6930-6943.
50. Takeda, S., Yamazaki, H., Seog, D. H., Kanai, Y., Terada, S. and Hirokawa, N. (2000). Kinesin superfamily protein 3 (KIF3) motor transports fodrin-associating vesicles important for neurite building. J. Cell Biol. 148, 1255-1265.
51. Tang, Y., Katuri, V., Iqbal, S., Narayan, T., Wang, Z., Lu, R. S., Mishra, L. and Mishra, B. (2002). ELF a beta-spectrin is a neuronal precursor cell marker in developing mammalian brain; structure and organization of the elf/beta-G spectrin gene. Oncogene 21, 5255-5267.
52. Tang, Y., Katuri, V., Dillner, A., Mishra, B., Deng, C. X. and Mishra, L. (2003). Disruption of transforming growth factor-beta signaling in ELF beta-spectrindeficient mice. Science 299, 574-577.
53. Tang, Y., Katuri, V., Srinivasan, R., Fogt, F., Redman, R., Anand, G., Said, A., Fishbein, T., Zasloff, M., Reddy, E. P. et al. (2005). Transforming growth factorbeta suppresses nonmetastatic colon cancer through Smad4 and adaptor protein ELF at an early stage of tumorigenesis. Cancer Res. 65, 4228-4237.
54. Thomas, P. S., Kim, J., Nunez, S., Glogauer, M. and Kaartinen, V. (2010). Neural crest cell-specific deletion of Rac1 results in defective cell-matrix interactions and severe craniofacial and cardiovascular malformations. Dev. Biol. 340, 613-625.
55. Tse, W. T., Tang, J., Jin, O., Korsgren, C., John, K. M., Kung, A. L., Gwynn, B., Peters, L. L. and Lux, S. E. (2001). A new spectrin, beta IV, has a major truncated isoform that associates with promyelocytic leukemia protein nuclear bodies and the nuclear matrix. J. Biol. Chem. 276, 23974-23985.
56. Tuvia, S., Buhusi, M., Davis, L., Reedy, M. and Bennett, V. (1999). Ankyrin-B is required for intracellular sorting of structurally diverse Ca2+ homeostasis proteins. J. Cell Biol. 147, 995-1008.
57. Van Essen, D. C. (1997). A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385, 313-318.
58. Woods, C. M. and Lazarides, E. (1985). Degradation of unassembled alpha- and betaspectrin by distinct intracellular pathways: regulation of spectrin topogenesis by betaspectrin degradation. Cell 40, 959-969.
59. Xu, J., Ziemnicka, D., Merz, G. S. and Kotula, L. (2000). Human spectrin Src homology 3 domain binding protein 1 regulates macropinocytosis in NIH 3T3 cells. J. Cell Sci. 113 Pt 21, 3805-3814.
60. Zhang, Y., Resneck, W. G., Lee, P. C., Randall, W. R., Bloch, R. J. and Ursitti, J. A. (2010). Characterization and expression of a heart-selective alternatively spliced variant of alpha II-spectrin, cardi+, during development in the rat. J. Mol. Cell Cardiol. 48, 1050-1059.
61. Ziemnicka-Kotula, D., Xu, J., Gu, H., Potempska, A., Kim, K. S., Jenkins, E. C., Trenkner, E. and Kotula, L. (1998). Identification of a candidate human spectrin Src homology 3 domain-binding protein suggests a general mechanism of association of tyrosine kinases with the spectrin-based membrane skeleton. J. Biol. Chem. 273, 13681-13692.