Evolution and origin of merlin, the product of the Neurofibromatosis type 2 (NF2) tumor-suppressor gene

BMC Evolutionary Biology

Volumn 5, Issue , 2005, Pages

  Golovnina, Kseniya ^a   Blinov, Alexander ^a   Akhmametyeva, Elena M ^b   Omelyanchuk, Leonid V ^a   Chang, Long Sheng ^b  

^a INSTITUTE OF CYTOLOGY AND GENETICS   (Russian Federation)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIONA; CIONA INTESTINALIS; INSECTA; MAMMALIA; METAZOA; UROCHORDATA; VERTEBRATA;

ACTIN; MERLIN; SERINE;

AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; BIOLOGY; CHEMISTRY; CIONA INTESTINALIS; DROSOPHILA; EXON; FISH; GENETICS; GENOME; HUMAN; INTRON; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; NEUROFIBROMATOSIS; PHOSPHORYLATION; PHYLOGENY; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; TUMOR SUPPRESSOR GENE;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CIONA INTESTINALIS; COMPUTATIONAL BIOLOGY; DROSOPHILA; EVOLUTION, MOLECULAR; EXONS; FISHES; GENES, TUMOR SUPPRESSOR; GENOME; HUMANS; INTRONS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; NEUROFIBROMATOSIS 2; NEUROFIBROMIN 2; PHOSPHORYLATION; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SERINE;

EID: 29144485489     PISSN: 14712148     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-5-69     Document Type: Article

References (88)

1. Dacks JB, Doolittle WF: Novel syntaxin gene sequences from Giardia, Trypanosoma and algae: implications for the ancient evolution of the eukaryotic endomembrane system. J Cell Sci 2002, 115:1635-1642.
2. Hsu S: Bioinformatics in reproductive biology - functional annotation based on comparative sequence analysis. J Rep Immunol 2004, 63:75-83.
3. NIH Consensus Statement on Acoustic Neuroma: Neurofibromatosis Res. Newsletter 1992, 8:1-7.
4. Bull. World Health Org: Prevention and control of neurofibromatosis: Memorandum from a joint WHO/NNFF meeting. 1992, 70:173-182.
5. Rouleau GA, Merel P, Luchtman M, Sanson M, Zucman J, Marineau C, Hoang-Xuan K, Demczuk S, Desmaze C, Plougastel B, Pulst SM, Le noir G, Bijlsma E, Fashold R, Dumanski J, de Jong P, Parry D, Eldridge R, Aurias A, Delattre O, Thomas G: Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature 1993, 363:515-521.
6. Trofatter JA, MacCollin MM, Rutter JL, Murrell JR, Duyai MP, Parry DM, Eldridge RE, Kley N, Menon AG, Pulaski K, Haase VH, Ambrose CM, Munroe D, Bove C, Haines JL, Martuza RL, MacDonald ME, Seizinger BR, Short MP, Buckner AJ, Gusella JF: A novel moezin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 1993, 72:791-800.
7. Algrain M, Arpin M, Louvard D: Wizardry at the cell cortex. Current Biol 1993, 3:451-454.
8. Tsukita S, Oishi K, Sato N, Sagara J, Kawai A, Tsukita S: ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeleton. J Cell Biol 1994, 126:391-401.
9. Takeuchi K, Kawashima A, Nagafuchi A, Tsukita S: Structural diversity of band 4.1 superfamily members. J Cell Sci 1994, 107:1921-1928.
10. Chishti AH, Kim AC, Marfatia SM, Lutchman M, Hanspal M, Jindal H, Liu SC, Low PS, Rouleau GA, Mohandas N, Chasis JA, Conboy JG, Gaskard P, Takakuwa Y, Huang SC, Benz EJ Jr, Bretcher A, Fenon RG, Gusella JF, Ramesh V, Solomon F, Marchesi VT, Tsukita S, Hoover KB: The FERM domain: a unique module involved in the linkage of the cytoplasmic proteins to the membrane. Trends Biochem Sci 1998, 23:281-282.
11. Hamada K, Shimizu T, Matsui T, Tsukita S, Hakoshima T: Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J 2000, 19:4449-4462.
12. Herrlich P, Morrison H, Sleeman J, Orian-Rousseau V, Konig H, Weg-Remers S, Ponta H: CD44 acts both as a growth- and invasiveness-promoting molecule and as a tumor-suppressing cofactor. Ann NY Acad Sci 2000, 910:106-118.
13. Morrison H, Sherman LS, Legg J, Banine F, Isacke C, Haipek CA, Gutmann DH, Ponta H, Herrlich P: The NF2 tumor suppressor gene product, merlin, mediates contact inhibition of growth through interactions with CD44. Genes Dev 2001, 15:968-980.
14. Hamada K, Shimizu T, Yonemura S, Tsukita Sh, Tsukita S, Hakoshima T: Structural basis of adhesion - molecule recognition by ERM proteins revealed by the crystal structure of the radixin - ICAM-2 complex. EMBO J 2003, 22:502-514.
15. Pearson MA, Reczek D, Bretscher A, Karplus PA: Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell 2000, 101:259-270.
16. Edwards SD, Keep NH: The 2.7 Å crystal structure of the activated FERM domain of moesin: an analysis of structural changes on activation. Biochemistry 2001, 40:7061-7068.
17. Kang BS, Cooper DR, Devedjiev Y, Derewenda U, Derewenda ZS: The structure of the FERM domain of merlin, the neurofibromatosis type 2 gene product. Acta Crystollogr Sec D 2002, 58:381-391.
18. Shimizu T, Seto A, Maita N, Hamada K, Tsukita Sh, Tsukita S, Hakoshima T: Structural basis for neurofibromatosis type2. J Biol Chem 2002, 277:10332-10336.
19. Turunen O, Sainio M, Jaaskelainen J, Carpen O, Vaheri A: Structure-function relationships in the ezrin family and the effect of tumor-associated point mutations in neurofibromatosis 2 protein. Biochim Biophys Acta 1998, 1387:1-16.
20. Turunen O, Wahlström T, Vaheri A: Ezrin has a COOH-terminal acting-binding site that is conserved in the ezrin protein family. J Cell Biol 1994, 126:1445-1453.
21. Gary R, Bretscher A: Ezrin self-association involves binding of an N-terminal domain to a normally masked C-terminal domain that includes the F-actin binding site. Mol Biol Cell 1995, 6:1061-1075.
22. Sainio M, Zhao F, Heiska L, Turunen O, den Bakker M, Zwarthoff E, Lutchman M, Rouleau GA, Jaaskelainen J, Vaheri A, Carpen O: Neurofibromatosis 2 tumor suppressor protein colocalizes with ezrin and CD44 and associates with actin-containing cytoskeleton. J Cell Sci 1997, 110:2249-2260.
23. Scoles DR, Huynh DP, Morcos PA, Coulsell ER, Robinson NG, Tamanoi F, Pulst SM: Neurofibromatosis 2 tumor suppressor schwannomin interacts with βII-spectrin. Nature Genet 1998, 18:354-359.
24. Neill GW, Crompton MR: Binding of the merlin-I product of the neurofibromatosis type 2 tumour suppressor gene to a novel site in beta-fodrin is regulated by association between merlin domains. Biochem J 2001, 358:727-735.
25. Bretscher A, Edwards K, Fehon RG: ERM proteins and merlin: integrators at the cell cortex. Nature Rev Mol Cell Biol 2002, 3:586-599.
26. Ramesh V: Merlin and ERM proteins in Schwann cells, neurons and growth cones. Nature Rev Neurosci 2004, 5:462-470.
27. McClatchey AI: Merlin and ERM proteins: unappreciated roles in cancer development? Nature Rev Cancer 2003, 3:877-883.
28. Gutmann DH, Haipek CA, Hoang Lu K: Neurofibromatosis 2 tumor suppressor protein, merlin, forms two functionally important intramolecular associations. J Neurosci Res 1999, 58:706-716.
29. Gutmann DH, Hirbe AC, Haipek CA: Functional analysis of neurofibromatosis 2 (NF2) missense mutations. Hum Mol Genet 2001, 10:1519-1529.
30. Shaw RJ, Paez JG, Curto M, Yaktine A, Pruitt WM, Saotome I, O'Bryan JP, Gupta V, Ratner N, Der CJ, Jacks T, McClatchey AI: The Nf2 tumor suppressor, merlin, functions in Rac-dependent signaling. Dev Cell 2001, 1:63-72.
31. Kissil JL, Johnson KC, Eckman MS, Jacks T: Merlin phosphorylation by p21-activated kinase 2 and effects of phosphorylation on merlin localization. J Biol Chem 2002, 277:10394-10399.
32. Xiao GH, Beeser A, Chernoff J, Testa JR: p21-activated kinase links Rac/Cdc42 signaling to merlin. J Biol Chem 2002, 277:883-886.
33. Alfthan K, Heiska L, Gronholm M, Renkema GH, Carpen O: Cyclic AMP-dependent protein kinase phosphorylates merlin at serine 518 independently of p21-activated kinase and promotes merlin-ezrin heterodimerization. J Biol Chem 2004, 279:18559-18566.
34. Surace EI, Haipek CA, Gutmann DH: Effect of merlin phosphorylation on neurofibromatosis 2 (NF2) gene function. Oncogene 2004, 23:580-587.
35. Rong R, Surace EI, Haipek CA, Gutmann DH, Ye K: Serine 518 phosphorylation modulates merlin intramolecular association and binding to critical effectors important for NF2 growth suppression. Oncogene 2004, 23:8447-8454.
36. Frosch PM, Frosch M, Pfister T, Schaad V, Bitter-Suermann D: Cloning and characterisation of an immunodominant major surface antigen of Echinococcus multilocularis. Mol Biochem Parasitol 1991, 48:121-130.
37. Frosch PM, Muhlschlegel F, Sygulla L, Hartmann M, Frosch M: Identification of a cDNA clone from the larval stage of Echinococcus granulosus with homologies to the E. multilocularis antigen EM10-expressing cDNA clone. Parasitol Res 1994, 80:703-705.
38. Kurtis JD, Ramirez BL, Wiest PM, Dong KL, El-Meanawy A, Petzke MM, Johnson JH, Edmison J, Maier RA Jr, Olds GR: Identification and molecular cloning of a 67-kilodalton protein in Schistosoma japonicum homologous to a family of actin-binding proteins. Infect Immun 1997, 65:344-347.
39. Hubert K, Cordero E, Frosch M, Solomon F: Activities of the EM10 protein from Echinococcus multilocularis in cultured mammalian cells demonstrate functional relationships to ERM family members. Cell Motil Cytoskeleton 1999, 42:178-188.
40. McCartney BM, Fehon RG: Distinct cellular and subcellular patterns of expression imply distinct functions for the Drosophila homologues of moesin and the neurofibromatosis 2 tumor suppressor, merlin. J Cell Biol 1996, 133:843-852.
41. Hansson CM, Ali H, Bruder CE, Fransson I, Kluge S, Andersson B, Roe BA, Menzel U, Dumanski JP: Strong conservation of the human NF2 locus based on sequence comparison in five species. Mamm Genome 2003, 14:526-536.
42. Chen Y-X, Gutmann DH, Haipek CA, Martinsen BJ, Bronner-Fraser M, Krull CE: Characterization of chicken Nf2/merlin indicates regulatory roles in cell proliferation and migration. Dev Dyn 2004, 229:541-54.
43. [http://www.tigr.org/tigr-scripts/tgi/est_report.pl?GB= CD797075&species=r_appendiculatus].
44. [http://www.tigr.org/tigr-scripts/tgi/est_report.pl?GB= BM291669&species=a_variegatum].
45. [http://www.tigr.org/tigr-scripts/tgi/est_report.pl?GB= CK190110&species=B.microplus].
46. [http://genome.wustl.edu/blast/client.pl].
47. Saitou N, Nei M: The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4:406-425.
48. Kumar S, Gadagkar SR: Efficiency of the neighbor-joining method in reconstructing deep and shallow evolutionary relationships in large phylogenies. J Mol Evol 2000, 51:544-53.
49. Kumar S, Tamura K, Jakobsen IB, Nei M: MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 2001, 17:1244-1245.
50. [http://www.tigr.org/tdb/e2k1/sma1/].
51. [http://www.wormbase.org/db/gene/gene?name=F42A10.2a;class=Transcript].
52. The C. elegans Sequencing Consortium: Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998, 282:2012-2018.
53. Adams MD, Celniker SE, Holt RA, Evans CA, et al.: The genome sequence of Drosophila melanogaster. Science 2000, 287:2185-2195.
54. Dehal P, Satou Y, Campbell RK, Chapman J, et al.: The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 2002, 298:2157-2167.
55. Stein LD, Bao Z, Blasiar D, Blumenthal T, et al.: The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 2003, 1:E45.
56. Foster JM, Kumar S, Ganatra MB, Kamal IH, Ware J, Ingram J, Pope-Chappell J, Guiliano D, Whitton C, Daub J, Blaxter ML, Slatko BE: Construction of bacterial artificial chromosome libraries from the parasitic nematode Brugia malayi and physical mapping of the genome of its Wolbachia endosymbiont. Int J Parasitol 2004, 34:733-746.
57. Matsui T, Maeda M, Doi Y, Yonemura S, Amano M, Kaibuchi K, Tsukita S: Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moezin (ERM) proteins and regulates their head-to-tail association. J Cell Biol 1998, 140:647-657.
58. Deguen B, Merel P, Goutebroze L, Giovannini M, Reggio H, Arpin M, Thomas G: Impaired interaction of naturally occurring mutant NF2 protein with actin-based cytoskeleton and membrane. Hum Mol Genet 1998, 7:217-226.
59. Xu H, Gutmann DH: Merlin differentially associates with the microtubule and acting cytoskeleton. J Neurosci Res 1998, 51:403-415.
60. Brault E, Gautreau A, Lamarine M, Callebaut I, Gilles T: Normal membrane localization and actin association of the NF2 tumor suppressor protein are dependent on folding of its N-terminal domain. J Cell Sci 2001, 114:1901-1912.
61. Roy C, Martin M, Mangeat P: A dual involvement of the amino terminal domain of ezrin in F- and G-actin binding. J Biol Chem 1997, 272:20088-20095.
62. Martin M, Roy C, Montcourrier P, Sahuquet A, Mangeat P: Three determinants in ezrin are responsible for cell extension activity. Mol Cell Biol 1997, 8:1543-1557.
63. LaJeunesse DR, McCartney BM, Fehon RG: Structural analysis of Drosophila merlin reveals functional domains important for growth control and subcellular localization. J Cell Biol 1998, 141:1589-1599.
64. Smith WJ, Nassar N, Bretscher A, Cerione RA, Karplus PA: Structure of the active N-terminal domain of ezrin. J Biol Chem 2003, 278:4949-4956.
65. Nakamura F, Amieva MR, Furthmayr H: Phosphorylation of threonine 558 in the carboxyl-terminal actin-binding domain of moesin by thrombin activation of human platelets. J Biol Chem 1995, 270:31377-31385.
66. Oshiro N, Fukata Y, Kaibuchi K: Phosphorylation of moesin by rho-associated kinase (Rho-kinase) plays a crucial role in the formation of microvilli-like structures. J Biol Chem 1998, 273:34663-34666.
67. Dard N, Louvet-Vallee S, Santa-Maria A, Maro B: Phosphorylation of ezrin on threonine T567 plays a crucial role during compaction in the mouse early embryo. Dev Biol 2004, 271:87-97.
68. Stokowski RP, Cox DR: Functional analysis of the neurofibromatosis type 2 protein by means of disease - causing point mutations. Am J Hum Genet 2000, 66:873-891.
69. [http://www.compbio.dundee.ac.uk/∼www-jpred/].
70. [http://www.tigr.org/tdb/e2k1/bma1/].
71. Zucman-Rossi J, Legoix P, Der Sarkissian H, Cheret G, Sor F, Bernardi A, Cazes L, Giraud S, Ollagnon E, Lenoir G, Thomas G: NF2 gene in neurofibromatosis type 2 patients. Hum Mol Genet 1998, 7:2095-2101.
72. Chang L-S, Akhmametyeva EM, Wu Y, Zhu L, Welling DB: Multiple transcription initiation sites, alternative splicing, and differential polyadenylation contribute to the complexity of human neurofibromatosis 2 transcripts. Genomics 2002, 79:63-76.
73. Arakawa H, Hayashi N, Nagase H, Ogawa M, Nakamura Y: Alternative splicing of the NF2 gene and its mutation analysis of breast and colorectal cancers. Hum Mol Genet 1994, 3:565-568.
74. Bianchi AB, Hara T, Ramesh V, Gao J, et al.: Mutations in transcript isoforms of the neurofibromatosis 2 gene in multiple human tumour types. Nature Genet 1994, 6:185-192.
75. Hara T, Bianchi AB, Seizinger BR, Kley N: Molecular cloning and characterization of alternatively spliced transcripts of the mouse neurofibromatosis 2 gene. Cancer Res 1994, 54:330-335.
76. Hitotsumatsu T, Kitamoto T, Iwaki T, Fukui M, Tateishi J: An exon 8-spliced out transcript of neurofibromatosis 2 gene is constitutively expressed in various human tissues. J Biochem (Tokyo) 1994, 116:1205-1207.
77. Pykett MJ, Murphy M, Harnish PR, George DL: The neurofibromatosis 2 (NF2) tumor suppressor gene encodes multiple alternatively spliced transcripts. Hum Mol Genet 1994, 3:559-564.
78. Nishi T, et al.: Neurofibromatosis 2 gene has novel alternative splicing which control intracellular protein binding. Int J Oncol 1997, 10:1025-1029.
79. Schmucker B, Tang Y, Kressel M: Novel alternatively spliced isoforms of the neurofibromatosis type 2 tumor suppressor are targeted to the nucleus and cytoplasmic granules. Hum Mol Genet 1999, 8:1561-1570.
80. Haase VH, Trofatter JA, MacCollin M, Tarttelin E, Gusella JF, Ramesh V: The murine NF2 homologue encodes a highly conserved merlin protein with alternative forms. Hum Mol Genet 1994, 3:407-411.
81. Huynh DP, Nechiporuk T, Pulst SM: Alternative transcripts in the mouse neurofibromatosis type 2 (NF2) gene are conserved and code for schwannomins with distinct C-terminal domains. Hum Mol Genet 1994, 3:1075-1079.
82. Gutmann DH, Wright DE, Geist RT, Snider WD: Expression of the neurofibromatosis 2 (NF2) gene isoforms during rat embryonic development. Hum Mol Genet 1995, 4:471-478.
83. [http://www.ncbi.nlm.nih.gov/BLAST].
84. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
85. [http://www.sanger.ac.uk/DataSearch].
86. [http://tigrblast.tigr.org/tgi/].
87. [http://www.ebi.uniprot.org/index.shtml].
88. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 15:4876-4882.