Dispensable role of protein 4.1B/DAL-1 in rodent adrenal medulla regarding generation of pheochromocytoma and plasmalemmal localization of TSLC1

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1793, Issue 3, 2009, Pages 506-515

  Ohno, Nobuhiko ^a   Terada, Nobuo ^a   Komada, Masayuki ^b   Saitoh, Sei ^a   Costantini, Frank ^c   Pace, Virgilio ^d   Germann, Paul Georg ^e   Weber, Klaus ^f   Yamakawa, Hisashi ^g   Ohara, Osamu ^g   Ohno, Shinichi ^a  

^a UNIVERSITY OF YAMANASHI   (Japan)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c NewYork Presbyterian Hospital   (United States)

^d Chemistry Section   (Italy)

^e Nycomed GmbH   (Germany)

^f RCC Ltd   (Switzerland)

^g KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

Adrenal medulla; Chromaffin cell; Pheochromocytoma; Protein 4.1B; TSLC1

Indexed keywords

ERYTHROCYTE BAND 4.1 PROTEIN; ERYTHROCYTE BAND 4.1 PROTEIN B; TUMOR SUPPRESSOR IN LUNG CANCER 1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ADRENAL MEDULLA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL MEMBRANE; CHROMAFFIN CELL; CONTROLLED STUDY; IMMUNOLOCALIZATION; MOUSE; NEUROFIBROMATOSIS; NONHUMAN; PHEOCHROMOCYTOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT;

ADRENAL GLAND NEOPLASMS; ADRENAL MEDULLA; ANIMALS; IMMUNOGLOBULINS; IN SITU HYBRIDIZATION; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; PHEOCHROMOCYTOMA; TUMOR SUPPRESSOR PROTEINS;

MUS; RODENTIA;

EID: 60549093353     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2009.01.005     Document Type: Article

References (62)

1. Braga V.M. Cell-cell adhesion and signalling. Curr. Opin. Cell Biol. 14 (2002) 546-556
2. Jamora C., and Fuchs E. Intercellular adhesion, signalling and the cytoskeleton. Nat. Cell Biol. 4 (2002) E101-E108
3. Perez-Moreno M., Jamora C., and Fuchs E. Sticky business: orchestrating cellular signals at adherens junctions. Cell 112 (2003) 535-548
4. Revenu C., Athman R., Robine S., and Louvard D. The co-workers of actin filaments: from cell structures to signals. Nat. Rev. Mol. Cell Biol. 5 (2004) 635-646
5. Deisenko-Nehrbass N., Oguievetskaia K., Goutebroze L., Galvez T., Yamakawa H., Ohara O., Carnaud M., and Girault J.A. Protein 4.1B associates with both Caspr/paranodin and Caspr2 at paranodes and juxtaparanodes of myelinated fibres. Eur. J. Neurosci. 17 (2003) 411-416
6. Ohara R., Yamakawa H., Nakayama M., and Ohara O. Type II brain 4.1 (4.1B/KIAA0987), a member of the protein 4.1 family, is localized to neuronal paranodes. Brain Res. Mol. Brain Res. 85 (2000) 41-52
7. Yamakawa H., and Ohara O. Comparison of mRNA and protein levels of four members of the protein 4.1 family: the type II brain 4.1/4.1B/KIAA0987 is the most predominant member of the protein 4.1 family in rat brain. Gene 248 (2000) 137-145
8. Ramez M., Blot-Chabaud M., Cluzeaud F., Chanan S., Patterson M., Walensky L.D., Marfatia S., Baines A.J., Chasis J.A., Conboy J.G., Mohandas N., and Gascard P. Distinct distribution of specific members of protein 4.1 gene family in the mouse nephron. Kidney Int. 63 (2003) 1321-1337
9. Terada N., Ohno N., Yamakawa H., Baba T., Fujii Y., Ohara O., and Ohno S. Protein 4.1B localizes on unmyelinated axonal membranes in the mouse enteric nervous system. Neurosci. Lett. 366 (2004) 15-17
10. Terada N., Ohno N., Yamakawa H., Baba T., Fujii Y., Zea Z., Ohara O., and Ohno S. Immunohistochemical study of protein 4.1B in the normal and W/W(v) mouse seminiferous epithelium. J. Histochem. Cytochem. 52 (2004) 769-777
11. Terada N., Ohno N., Yamakawa H., Seki G., Fujii Y., Baba T., Ohara O., and Ohno S. Immunoelectron microscopic localization of protein 4.1B in proximal S1 and S2 tubules of rodent kidneys. Med. Electron Microsc. 37 (2004) 45-51
12. Tran Y.K., Bogler O., Gorse K.M., Wieland I., Green M.R., and Newsham I.F. A novel member of the NF2/ERM/4.1 superfamily with growth suppressing properties in lung cancer. Cancer Res. 59 (1999) 35-43
13. Gutmann D.H., Donahoe J., Perry A., Lemke N., Gorse K., Kittiniyom K., Rempel S.A., Gutierrez J.A., and Newsham I.F. Loss of DAL-1, a protein 4.1-related tumor suppressor, is an important early event in the pathogenesis of meningiomas. Hum. Mol. Genet. 9 (2000) 1495-1500
14. Charboneau A.L., Singh V., Yu T., and Newsham I.F. Suppression of growth and increased cellular attachment after expression of DAL-1 in MCF-7 breast cancer cells. Int. J. Cancer 100 (2002) 181-188
15. Ohno N., Terada N., Murata S., Yamakawa H., Newsham I.F., Katoh R., Ohara O., and Ohno S. Immunolocalization of protein 4.1B/DAL-1 during neoplastic transformation of mouse and human intestinal epithelium. Histochem. Cell Biol. 122 (2004) 579-586
16. Singh P.K., Gutmann D.H., Fuller C.E., Newsham I.F., and Perry A. Differential involvement of protein 4.1 family members DAL-1 and NF2 in intracranial and intraspinal ependymomas. Mod. Pathol. 15 (2002) 526-531
17. Wong S.Y., Haack H., Kissil J.L., Barry M., Bronson R.T., Shen S.S., Whittaker C.A., Crowley D., and Hynes R.O. Protein 4.1B suppresses prostate cancer progression and metastasis. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 12784-12789
18. Heller G., Fong K.M., Girard L., Seidl S., End-Pfutzenreuter A., Lang G., Gazdar A.F., Minna J.D., Zielinski C.C., and Zochbauer-Muller S. Expression and methylation pattern of TSLC1 cascade genes in lung carcinomas. Oncogene 25 (2006) 959-968
19. Heller G., Geradts J., Ziegler B., Newsham I., Filipits M., Markis-Ritzinger E.M., Kandioler D., Berger W., Stiglbauer W., Depisch D., Pirker R., Zielinski C.C., and Zochbauer-Muller S. Downregulation of TSLC1 and DAL-1 expression occurs frequently in breast cancer. Breast Cancer Res. Treat. 103 (2007) 283-291
20. Houshmandi S.S., Surace E.I., Zhang H.B., Fuller G.N., and Gutmann D.H. Tumor suppressor in lung cancer-1 (TSLC1) functions as a glioma tumor suppressor. Neurology 67 (2006) 1863-1866
21. Kuramochi M., Fukuhara H., Nobukuni T., Kanbe T., Maruyama T., Ghosh H.P., Pletcher M., Isomura M., Onizuka M., Kitamura T., Sekiya T., Reeves R.H., and Murakami Y. TSLC1 is a tumor-suppressor gene in human non-small-cell lung cancer. Nat. Genet. 27 (2001) 427-430
22. Murakami Y. Involvement of a cell adhesion molecule, TSLC1/IGSF4, in human oncogenesis. Cancer Sci. 96 (2005) 543-552
23. Yageta M., Kuramochi M., Masuda M., Fukami T., Fukuhara H., Maruyama T., Shibuya M., and Murakami Y. Direct association of TSLC1 and DAL-1, two distinct tumor suppressor proteins in lung cancer. Cancer Res. 62 (2002) 5129-5133
24. Yi C., McCarty J.H., Troutman S.A., Eckman M.S., Bronson R.T., and Kissil J.L. Loss of the putative tumor suppressor band 4.1B/Dal1 gene is dispensable for normal development and does not predispose to cancer. Mol. Cell. Biol. 25 (2005) 10052-10059
25. Tsujiuchi T., Sugata E., Masaoka T., Onishi M., Fujii H., Shimizu K., and Honoki K. Expression and DNA methylation patterns of Tslc1 and Dal-1 genes in hepatocellular carcinomas induced by N-nitrosodiethylamine in rats. Cancer Sci. 98 (2007) 943-948
26. Pace V., Perentes E., and Germann P.G. Pheochromocytomas and ganglioneuromas in the aging rats: morphological and immunohistochemical characterization. Toxicol. Pathol. 30 (2002) 492-500
27. Smith-Hicks C.L., Sizer K.C., Powers J.F., Tischler A.S., and Costantini F. C-cell hyperplasia, pheochromocytoma and sympathoadrenal malformation in a mouse model of multiple endocrine neoplasia type 2B. EMBO J. 19 (2000) 612-622
28. Komada M., and Soriano P. Hrs, a FYVE finger protein localized to early endosomes, is implicated in vesicular traffic and required for ventral folding morphogenesis. Genes Dev. 13 (1999) 1475-1485
29. Li Z., Ohno N., Terada N., and Ohno S. Immunolocalization of serum proteins in living mouse glomeruli under various hemodynamic conditions by "in vivo cryotechnique". Histochem. Cell Biol. 126 (2006) 399-406
30. Ohno N., Terada N., and Ohno S. Histochemical analyses of living mouse liver under different hemodynamic conditions by "in vivo cryotechnique". Histochem. Cell Biol. 126 (2006) 389-398
31. Terada N., Ohno N., Yamakawa H., Ohara O., Liao X., Baba T., and Ohno S. Immunohistochemical study of a membrane skeletal molecule, protein 4.1G, in mouse seminiferous tubules. Histochem. Cell Biol. 124 (2005) 303-311
32. Ohno N., Terada N., Saitoh S., and Ohno S. Extracellular space in mouse cerebellar cortex revealed by in vivo cryotechnique. J. Comp. Neurol. 505 (2007) 292-301
33. Gascard P., Parra M.K., Zhao Z., Calinisan V.R., Nunomura W., Rivkees S.A., Mohandas N., and Conboy J.G. Putative tumor suppressor protein 4.1B is differentially expressed in kidney and brain via alternative promoters and 5′ alternative splicing. Biochim. Biophys. Acta 1680 (2004) 71-82
34. Kannan R., Grant N.J., Aunis D., and Langley K. SNAP-25 is differentially expressed by noradrenergic and adrenergic chromaffin cells. FEBS Lett. 385 (1996) 159-164
35. Shingai T., Ikeda W., Kakunaga S., Morimoto K., Takekuni K., Itoh S., Satoh K., Takeuchi M., Imai T., Monden M., and Takai Y. Implications of nectin-like molecule-2/IGSF4/RA175/SgIGSF/TSLC1/SynCAM1 in cell-cell adhesion and transmembrane protein localization in epithelial cells. J. Biol. Chem. 278 (2003) 35421-35427
36. Fritz A., Walch A., Piotrowska K., Rosemann M., Schaffer E., Weber K., Timper A., Wildner G., Graw J., Hofler H., and Atkinson M.J. Recessive transmission of a multiple endocrine neoplasia syndrome in the rat. Cancer Res. 62 (2002) 3048-3051
37. Chan S.A., Polo-Parada L., Landmesser L.T., and Smith C. Adrenal chromaffin cells exhibit impaired granule trafficking in NCAM knockout mice. J. Neurophysiol. 94 (2005) 1037-1047
38. Parra M., Gascard P., Walensky L.D., Gimm J.A., Blackshaw S., Chan N., Takakuwa Y., Berger T., Lee G., Chasis J.A., Snyder S.H., Mohandas N., and Conboy J.G. Molecular and functional characterization of protein 4.1B, a novel member of the protein 4.1 family with high level, focal expression in brain. J. Biol. Chem. 275 (2000) 3247-3255
39. Garcia A.G., Garcia-De-Diego A.M., Gandia L., Borges R., and Garcia-Sancho J. Calcium signaling and exocytosis in adrenal chromaffin cells. Physiol. Rev. 86 (2006) 1093-1131
40. Benedeczky I., and Somogyi P. Ultrastructure of the adrenal medulla of normal and insulin-treated hamsters. Cell Tissue Res. 162 (1975) 541-550
41. Kikuchi S., Yamada D., Fukami T., Maruyama T., Ito A., Asamura H., Matsuno Y., Onizuka M., and Murakami Y. Hypermethylation of the TSLC1/IGSF4 promoter is associated with tobacco smoking and a poor prognosis in primary nonsmall cell lung carcinoma. Cancer 106 (2006) 1751-1758
42. Wakayama T., Ohashi K., Mizuno K., and Iseki S. Cloning and characterization of a novel mouse immunoglobulin superfamily gene expressed in early spermatogenic cells. Mol. Reprod. Dev. 60 (2001) 158-164
43. van der W.L., Arends M.J., Chausiaux O.E., Ellis P.J., Lange U.C., Surani M.A., Affara N., Murakami Y., Adams D.J., and Bradley A. Loss of TSLC1 causes male infertility due to a defect at the spermatid stage of spermatogenesis. Mol. Cell. Biol. 26 (2006) 3595-3609
44. Yamada D., Yoshida M., Williams Y.N., Fukami T., Kikuchi S., Masuda M., Maruyama T., Ohta T., Nakae D., Maekawa A., Kitamura T., and Murakami Y. Disruption of spermatogenic cell adhesion and male infertility in mice lacking TSLC1/IGSF4, an immunoglobulin superfamily cell adhesion molecule. Mol. Cell. Biol. 26 (2006) 3610-3624
45. Kuns R., Kissil J.L., Newsham I.F., Jacks T., Gutmann D.H., and Sherman L.S. Protein 4.1B expression is induced in mammary epithelial cells during pregnancy and regulates their proliferation. Oncogene 24 (2005) 6502-6515
46. Terada N., Ohno N., Saitoh S., Seki G., Komada M., Suzuki T., Yamakawa H., Soleimani M., and Ohno S. Interaction of membrane skeletal protein, protein 4.1B and p55, and sodium bicarbonate cotransporter1 in mouse renal S1-S2 proximal tubules. J. Histochem. Cytochem. 55 (2007) 1199-1206
47. McCarty J.H., Cook A.A., and Hynes R.O. An interaction between {alpha}v{beta}8 integrin and Band 4.1B via a highly conserved region of the Band 4.1 C-terminal domain. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 13479-13483
48. Gollan L., Sabanay H., Poliak S., Berglund E.O., Ranscht B., and Peles E. Retention of a cell adhesion complex at the paranodal junction requires the cytoplasmic region of Caspr. J. Cell Biol. 157 (2002) 1247-1256
49. Coupland R.E. Electron microscopic observations on the structure of the rat adrenal medulla. I. The ultrastructure and organization of chromaffin cells in the normal adrenal medulla. J. Anat. 99 (1965) 231-254
50. Lacy P.E., and Hartroft W.S. Electron microscopy of the islets of Langerhans. Ann. N. Y. Acad. Sci. 82 (1959) 287-301
51. Terada N., Ohno N., Yamakawa H., Baba T., Fujii Y., Christofori G., Ohara O., and Ohno S. Protein 4.1B in mouse islets of Langerhans and beta-cell tumorigenesis. Histochem. Cell Biol. 120 (2003) 277-283
52. Parra M., Gee S., Chan N., Ryaboy D., Dubchak I., Mohandas N., Gascard P.D., and Conboy J.G. Differential domain evolution and complex RNA processing in a family of paralogous EPB41 (protein 4.1) genes facilitate expression of diverse tissue-specific isoforms. Genomics 84 (2004) 637-646
53. Robb V.A., Gerber M.A., Hart-Mahon E.K., and Gutmann D.H. Membrane localization of the U2 domain of Protein 4.1B is necessary and sufficient for meningioma growth suppression. Oncogene 24 (2005) 1946-1957
54. Jiang W., and Newsham I.F. The tumor suppressor DAL-1/4.1B and protein methylation cooperate in inducing apoptosis in MCF-7 breast cancer cells. Mol. Cancer 5 (2006) 4
55. Cavanna T., Pokorna E., Vesely P., Gray C., and Zicha D. Evidence for protein 4.1B acting as a metastasis suppressor. J. Cell Sci. 120 (2007) 606-616
56. Jimenez C., Cote G., Arnold A., and Gagel R.F. Review: should patients with apparently sporadic pheochromocytomas or paragangliomas be screened for hereditary syndromes?. J. Clin. Endocrinol. Metab. 91 (2006) 2851-2858
57. Karagiannis A., Mikhailidis D.P., Athyros V.G., and Harsoulis F. Pheochromocytoma: an update on genetics and management. Endocr. Relat Cancer 14 (2007) 935-956
58. Fukuhara H., Masuda M., Yageta M., Fukami T., Kuramochi M., Maruyama T., Kitamura T., and Murakami Y. Association of a lung tumor suppressor TSLC1 with MPP3, a human homologue of Drosophila tumor suppressor Dlg. Oncogene 22 (2003) 6160-6165
59. Sun C.X., Robb V.A., and Gutmann D.H. Protein 4.1 tumor suppressors: getting a FERM grip on growth regulation. J. Cell. Sci. 115 (2002) 3991-4000
60. Walensky L.D., Blackshaw S., Liao D., Watkins C.C., Weier H.U., Parra M., Huganir R.L., Conboy J.G., Mohandas N., and Snyder S.H. A novel neuron-enriched homolog of the erythrocyte membrane cytoskeletal protein 4.1. J. Neurosci. 19 (1999) 6457-6467
61. Delhommeau F., Vasseur-Godbillon C., Leclerc P., Schischmanoff P.O., Croisille L., Rince P., Morinière M., Benz E.J., Tchernia G., Tamagnini G., Ribeiro L., Delaunay J., and Baklouti F. A splicing alteration of 4.1R pre-mRNA generates 2 protein isoforms with distinct assembly to spindle poles in mitotic cells. Blood 100 (2002) 2629-2636
62. Shi Z.T., Afzal V., Coller B., Patel D., Chasis J.A., Parra M., Lee G., Paszty C., Stevens M., Walensky L., Peters L.L., Mohandas N., Rubin E., and Conboy J.G. Protein 4.1R-deficient mice are viable but have erythroid membrane skeleton abnormalities. J. Clin. Invest. 103 (1999) 331-340