A nonerythroid isoform of protein 4.1R interacts with the nuclear mitotic apparatus (NuMA) protein

Journal of Cell Biology

Volumn 145, Issue 1, 1999, Pages 29-43

  Mattagajasingh, Subhendra N ^a   Huang, Shu Ching ^a   Hartenstein, Julia S ^a   Snyder, Michael ^b   Marchesi, Vincent T ^c   Benz Jr , Edward J ^a,d  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Dynactin; Dynein; Mitotic spindle; NuMA; Protein 4.1R

Indexed keywords

CELL PROTEIN; DYNACTIN; DYNEIN ADENOSINE TRIPHOSPHATASE; EPITOPE; ERYTHROCYTE BAND 4.1 PROTEIN; ISOPROTEIN; NUCLEAR MITOTIC APPARATUS PROTEIN; NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL CYCLE PHASE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; CYTOARCHITECTURE; HUMAN; HUMAN CELL; MITOSIS SPINDLE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, NUCLEAR; BINDING SITES; CELL CYCLE; CELL LINE; CYTOSKELETAL PROTEINS; DOGS; DYNEIN ATPASE; HELA CELLS; HUMANS; INTERPHASE; KIDNEY; MACROMOLECULAR SUBSTANCES; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MITOTIC SPINDLE APPARATUS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEUROPEPTIDES; NUCLEAR MATRIX-ASSOCIATED PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN ISOFORMS; RECOMBINANT FUSION PROTEINS; RNA SPLICING; SACCHAROMYCES CEREVISIAE;

ANIMALIA;

EID: 0033526060     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.1.29     Document Type: Article

References (75)

1. Anderson, R.A., and R.E. Lovrien. 1984. Glycophorin is linked by band 4.1 to the human erythrocyte membrane skeleton. Nature. 307:655-658.
2. Anderson, R.A., I. Correas, C. Mazzucco, J.D. Castle, and V.T. Marchesi. 1988. Tissue-specific analogues of erythrocyte protein 4.1 retain functional domains. J. Cell. Biochem. 37:269-284.
3. Baklouti, F., S.C. Huang, T.J. Vulliamy, J.D. Delaunay, and E.J. Benz, Jr. 1997. Organization of the human protein 4.1 genomic locus: new insights into the tissue-specific alternative splicing of the pre-mRNA. Genomics. 39:289-302.
4. Becker, P.S., M.A. Schwartz, J.S. Morrow, and S.E. Lux. 1990. Radiolabel-transfer cross-linking demonstrates that protein 4.1 binds to the N-terminal region of β spectrin and to actin in binary interactions. Eur. J. Biochem. 193:827-836.
5. Chasis, J.A., L. Coulombel, J. Conboy, S. McGee, K. Andrews, Y.W. Kan, and N. Mohandas. 1993. Differentiation-associated switches in protein 4.1 expression: synthesis of multiple structural isoforms during normal human erythropoieses. J. Clin. Invest. 91:329-338.
6. Chasis, J.A., L. Coulombel, S. McGee, G. Lee, G. Tchernia, J. Conboy, and N. Mohandas. 1996. Differential use of protein 4.1 translation sites during erythropoiesis: implications for a mutation-induced stage-specific deficiency of protein 4.1 during erythroid development. Blood. 87:5324-5331.
7. Cohen, C.M., S.F. Foley, and C. Korsgen. 1982. A protein immunologically related to erythrocyte band 4.1 is found on stress fibers of non-erythroid cells. Nature. 299:648-650.
8. Compton, D.A., and D.W. Cleveland. 1993. NuMA is required for the proper completion of mitosis. J. Cell Biol. 120:947-957.
9. Compton, D.A., I. Szilak, and D.W. Cleveland. 1992. Primary structure of NuMA, an intranuclear protein that defines a novel pathway for segregation of proteins at mitosis. J. Cell Biol. 116:1395-1408.
10. Conboy, J.G., J. Chan, J.A. Chasis, Y.W. Kan, and N. Mohandas. 1991. Tissue- and development-specific alternative RNA splicing regulates expression of multiple isoforms of erythroid membrane protein 4.1. J. Biol. Chem. 266: 8273-8280.
11. Correas, I., and J. Avila. 1988. Erythrocyte protein 4.1 associates with tubulin. Biochem. J. 255:217-221.
12. Correas, I., T.L. Leto, D.W. Speicher, and V.T. Marchesi. 1986. Identification of the functional site of erythrocyte protein 4.1 involved in spectrin-actin associations. J. Biol. Chem. 261:3310-3315.
13. Cox, K.H., T.L. Adair-Kirk, and J.V. Cox. 1995. Four variant chicken erythroid anion exchangers. Roles of the alternative N-terminal sequences in intracellular targeting in transfected human erythroleukemia cells. J. Biol. Chem. 270:19752-19760.
14. De Carcer, G., M.J. Lallena, and I. Correas. 1995. Protein 4.1 is a component of the nuclear matrix of mammalian cells. Biochem. J. 312:871-877.
15. Dionne, M.A., L. Howard, and D.A. Compton. 1999. NuMA is a component of an insoluble matrix at mitotic spindle poles. Cell Motil. Cyloskel. In press.
16. Discher, D.E., M. Parra, J.G. Conboy, and N. Mohandas. 1993. Mechanochemistry of the alternatively spliced spectrin-actin binding domain in membrane skeletal protein 4.1. J. Biol. Chem. 268:7186-7195.
17. Doxsey, A.T., P. Stein, L. Evans, P.D. Calarco, and M. Kirschner. 1994. Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell. 76:639-650.
18. Gaglio, T., A. Saredi, and D.A. Compton. 1995. NuMA is required for the organization of microtubules into asterlike mitotic arrays. J. Cell Biol. 131:693-708.
19. Gaglio, T., A. Saredi, J.B. Bingham, M.J. Hasbani, S.R. Gill, T.A. Schroer, and D.A. Complon. 1996. Opposing motor activities are required for the organization of the mammalian mitotic spindle pole. J. Cell Biol. 135:399-414.
20. Gaglio, T., M.A. Dionne, and D.A. Compton. 1997. Mitotic spindle poles are organized by structural and motor proteins in addition to centrosomes. J. Cell Biol. 138:1055-1066.
21. Gee, M.A., J.E. Heuser, and R.B. Vallee. 1997. An extended microtubule-binding structure within the dynein motor domain. Nature. 390:636-639.
22. Granger, B.L., and E. Lazarides. 1984. Membrane skeletal protein 4.1 of avian erythrocytes is composed of multiple variants that exhibit tissue-specific expression. Cell. 37:595-607.
23. Granger, B.L., and E. Lazarides. 1985. Appearance of new variants of membrane skeletal protein 4.1 during terminal differentiation of avian erythroid and lenticular cells. Nature. 313:238-241.
24. Gueth-Hallonet, C., K. Weber, and M. Osborn. 1996. NuMA: a bipartite nuclear location signal and other functional properties of the tail domain. Exp. Cell Res. 225:207-218.
25. He, D., C. Zeng, and B.R. Brinkley. 1995. Nuclear matrix proteins as structural and functional components of the mitotic apparatus. Int. Rev. Cytol. 162B:1-74.
26. Heald, R., R. Tournebize, A. Habermann, E. Karsenti, and A. Hyman. 1997. Spindle assembly in Xenopus egg extracts: Respective roles of centrosomes and microtubule self-organization. J. Cell Biol. 138:615-628.
27. Hemming, N.J., D.J. Anstee, W.J. Mawby, M.E. Reid, and M.J.A. Tanner. 1994. Localization of the protein 4.1-bindingsite on human erythrocyte glycophorin C and D. Biochem. J. 299:191-196.
28. Himmler, A., D. Preshsel, M.W. Kirschner, and D.W. Martin. 1989. Tau consists of a set of proteins with repeated C-terminal microtubule-binding domains and variable N-terminal domains. Mol. Cell. Biol. 9:1381-1388.
29. Home, W.C., S.C. Huang, P.S. Baker, T.K. Tang, and E.J. Benz, Jr. 1993. Tissue-specific alternative splicing of protein 4.1 inserts an exon necessary for formation of the ternary complex with erythrocyte spectrin and F-actin. Blood. 82:2558-2563.
30. Houliston, E., R. Le Guellec, M. Kress, M. Philippe, and K. Le Guellec. 1994. The kinesin-related protein Eg5 associates with both interphase and spindle microtubules during Xenopus early development. Dev. Biol. 164:147-159.
31. Huang, S.C., F. Baklouti, T.K. Tang, and E.J. Benz, Jr. 1992. Differential utilization of translation initiation sites in alternatively spliced mRNAs arising from the protein 4.1 gene. Trans. Assoc. Am. Physicians. 105:165-171.
32. Huang, J.P., C.J.C. Tang, G.H. Kou, V.T. Marchesi, E.J. Benz, Jr., and T.K. Tang. 1993. Genomic structure of the locus encoding protein 4.1: structural basis for complex combinational pattern of tissue-specific alternative RNA splicing. J. Biol. Chem. 268:3758-3766.
33. Jons, T., and D. Drenckhahn. 1992. Identification of the binding interface involved in linkage of cytoskeletal protein 4.1 to the erythrocyte anion exchanger. EMBO (Eur. Mol. Biol. Organ.) J. 11:2863-2867.
34. Kallajoki, M., K. Weber, and M. Osborn. 1991. A 210 kD nuclear matrix protein is a functional part of the mitotic spindle; a microinjection study using SPN monoclonal antibodies. EMBO (Eur. Mol. Biol. Organ.) J. 10:3351-3362.
35. Krauss, S.W., J.A. Chasis, C. Rogers, N. Mohandas, G. Krockmalnic, and S. Penman. 1997a. Structure of protein 4.1 is located in mammalian centrosomes. Proc. Natl. Acad. Sci. USA. 94:7297-7302.
36. Krauss, S.W., C.A. Larabell, S. Lockett, P. Gascard, S. Penman, M. Narla, and J.A. Chasis. 1997b. Structural protein 4.1 in the nucleus of human cells: dynamic rearrangements during cell division. J. Cell Biol. 137:275-289.
37. Kuriyama, R.M., R. Kofron, T. Essner, S. Kato, C.K. Dragas-Granoic, A. Omoto, and A. Khodjakov. 1995. Characterization of a minus end-directed kinesin-like motor protein from cultured mammalian cells. J. Cell Biol. 129: 1049-1059.
38. Lallena, M.J., and I. Correas. 1997. Transcription-dependent redistribution of nuclear protein 4.1 to SC35-enriched nuclear domains. J. Cell Sci. 110:239-247.
39. Leque, CM., M.J. Lallena, M.A. Alonso, and I. Correas. 1998. An alternative domain determines nuclear localization in multifunctional protein 4.1. J. Biol. Chem. 273:11643-11649.
40. Leto, T.L., B.M. Pratt, and J.A. Madri. 1986. Mechanisms of cytoskeleton regulation: modulation of aortic endothelial cell protein hand 4.1 by the extracellular matrix. J. Cell Physiol. 127:423-431.
41. Lewis, S.A., D. Wang, and N.J. Cowan. 1988. Microtubule-associated protein MAP2 shares a microtubule-binding motif with tau protein. Science. 242: 936-939.
42. Lue, R.A., S.M. Marfatia, D. Branton, and A.H. Chishti. 1994. Cloning and characterization of hdlg: the human homologue of the Drosophila discs large tumor suppresser binds to protein 4.1. Proc. Natl. Acad. Sci. USA. 91:9818-9822.
43. Madri, J.A., B.M. Pratt, and J. Yannariello-Brown. 1988. Endothelial cell-extracellular matrix interactions. In Endothelial Cell Biology in Health and Disease. N. Simionescu, and M. Simionescu, editors. Plenum Press/New York. 167-188.
44. Maekawa, T., and R. Kuriyama. 1993. Primary structure and microtubule-interacting domain of the SP-H antigen: a mitotic map located at the spindle pole and characterized as a homologous protein to NuMA. J. Cell Sci. 105:589-600.
45. Malchiodi-Albedi, F. M. Ceccarini, J.C. Winkelman, J.S. Morrow, and T.C. Petrucci. 1993. The 270 kD splice variant of erythrocyte [beta]-spectrin ([beta]1[Sigma]2) segregates in vivo and in vitro to specific domains of cerebellar neurons. J. Cell Sci. 106:67-78.
46. Marfatia, S.M., R. Lue, D. Branton and A.H. Chishti. 1995. Identification of the protein 4.1 binding interface on glycophorin C and p55, a homologue of the Drosophila discs-large tumor suppresser protein. J. Biol. Chem. 270:715-719.
47. Mattagajasingh, S.N., and H.P. Misra. 1996. Mechanisms of the carcinogenic chromium(VI)-induced DNA-protein cross-linking and their characterization in cultured intact human cells. J. Biol. Chem. 271:33550-33560.
48. Merdes, A., K. Ramyar, L.D. Vechio, and D.W. Cleveland. 1996. A complex of NuMA and cytoplasmic dynein is essential for mitotic spindle assembly. Cell. 87:447-458.
49. Merdes, A., and D.W. Cleveland. 1998. The role of NuMA in the interphase nucleus. J. Cell Sci. 111:71-79.
50. Morris, M.B., and S.E. Lux. 1995. Characterization of the binary interaction between human erythrocyte protein 4.1 and actin. Eur. J. Biochem. 231: 644-650.
51. O'Conner, P.M., and J. Jackman. 1995. Synchronization of mammalian cells. In Cell Cycle-Materials and Methods. M. Pogans, editor. Spinger-Verlag, New York. 63-74.
52. Parra, M., P. Gascard, L.D. Walensky, S.H. Snyder, N. Mohandas, and J.G. Conboy. 1998. Cloning and characterization of 4.1G (EPB41L2), a new member of the skeletal protein 4.1 (EPB41) gene family. Genomics. 49:298-306.
53. Pasternack, G.R., and R.H. Racusen. 1989. Erythrocyte protein 4.1 binds and regulates myosin. Proc. Natl. Acad. Sci. USA. 86:9712-9716.
54. Pasternack, G.R., R.A. Anderson, T.L. Leto, and V.T. Marchesi. 1984. Interactions between protein 4.1 and band 3. An alternative binding site for an element of the membrane skeleton. J. Biol. Chem. 260:3676-3683.
55. Pfarr, C.M., M. Coue, P.M. Grissom, T.S. Hays, M.E. Porter, and J.R. McIntosh. 1990. Cyloplasmic dynein is localized to kinetochores during mitosis. Nature. 345:263-265.
56. Price, C.M., and D.E. Pettijohn. 1986. Distribution of the nuclear mitotic apparatus protein (NuMA) during mitosis and nuclear assembly. Exp. Cell Res. 166:295-311.
57. Sammons, D.W., L.D. Adams, and E.E. Nishiziwa. 1981. Ultrasensitive silver based color staining of polypeptides in polyacrylamide gels. Electrophoresis. 2:135-141.
58. Saredi, A., L. Howard, and D.A. Compton. 1996. NuMA assembles into an extensive filamentous structure when expressed in the cell cytoplasm. J. Cell Sci. 109:619-630.
59. Saunders, R.D.C., M. Avides, T. Howard, C. Gonzalez, and D.M. Glover. 1997. The Drosophila gene abnormal spindle encodes a novel microtubule-associated protein that associates with the polar regions of the mitotic spindle. J. Cell Biol. 137:881-890.
60. Stearns, T., and M. Kirschner. 1994. In vitro reconstitution of centrosome assembly and function: the central role of-γ-tubulin. Cell. 76:623-637.
61. Steur, E.R., L. Wordeman, T.A. Schroer, and M.P. Sheetz. 1990. Localization of cytoplasmic dynein to mitotic spindles and kinetochores. Nature. 345: 266-268.
62. Subrahmanyam, G., P. Bertics, and R. Anderson. 1991. Phosphorylation of protein 4.1 on tyrosine-418 modulates its function in vitro. Proc. Natl. Acad. Sci. USA. 88:5222-5226.
63. 2+-dependent regulation of the spectrin/aclin interaction by calmodulin and protein 4.1. J. Biol. Chem. 266:1134-1140.
64. Tang, T.K., T.L. Leto, I. Correas, M.A. Alonso, V.T. Marchesi, and E.J. Benz, Jr. 1988. Selective expression of an erythroid-specific isoform of protein generates two proteins. Proc. Natl. Acad. Sci. USA. 85:3713-3717.
65. Tang, T.K., Z. Quin, V.T. Marchesi, and E.J. Benz, Jr. 1990. Heterogeneity of mRNA and protein products arising from the protein 4.1 gene in erythroid and nonerythroid tissues. J. Cell Biol. 110:617-624.
66. Tang, T.K., C.J.C. Tang, Y.L. Chen, and C.W. Wu. 1993. Nuclear proteins of the bovine esophageal epithelium: the NuMA gene gives rise to multiple mRNAs and gene products reactive with monoclonal antibody W1. J. Cell Sci. 104:249-260.
67. Tang, T.K., C.J.C. Tang, Y.J. Chao, and C.W. Wu. 1994. Nuclear mitotic apparatus protein (NuMA): spindle association, nuclear targeting, and differential subcellular localization of various NuMA isoforms. J. Cell Sci. 107:1389-1402.
68. Tyler, J.M., W.R. Hargeaves, and D. Branton. 1979. Purificalion of spectrin-binding proleins: biochemical and electron microscopic evidence for site-specific reassociation between spectrin and bands 2.1 and 4.1. Proc. Natl. Acad. Sci. USA. 76:5192-5196.
69. Ungewickell, E., P.M. Bennet, R. Calvert, V. Ohanian, and W.B. Gratzer. 1979. In vitro formation of a complex between cytoskeletal proteins of human erythrocyte. Nature. 280:811-814.
70. Walensky, L.D., P. Gascard, M.E. Fields, S. Blackshaw, J.G. Conboy, N. Mohandas, and S.H. Snyder. 1998. The 13-kD FK506 binding protein, FKBP13, interacts with a novel homologue of the erythrocyte membrane cytoskeletal protein 4.1. J. Cell Biol. 141:143-153.
71. Glued component of the dynactin complex binds to both microtubule and the actin related protein centractin (Arp-1). Proc. Natl. Acad. Sci. USA. 92:1634-1638.
72. Yang, C.H., and M. Snyder. 1992. The nuclear-mitotic apparatus protein is im-portant in the establishment and maintenance of the bipolar mitotic spindle apparatus. Mol. Biol. Cell. 3:1259-1267.
73. Yang, J.T., R.A. Layman, and I.S.B. Goldstein. 1989. A three domain structure of the kinesin heavy chain revealed by DNA sequence and microtubule-binding analysis. Cell. 56:879-889.
74. Zahler, R., M. Gilmore-Habert, J.C. Baldwin, K. Franco, and E.J. Benz, Jr. 1993. Expression of a isoforms of the Na-K-ATPase in human heart. Biochim. Biophys. Acta. 1149:189-194.
75. Zeng, C., D. He, and B.R. Brinkley. 1994. Localization of NuMA protein isoforms in the nuclear matrix of mammalian cells. Cell Motil. Cytoskel. 29: 167-176.