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Published in: Cellular Oncology 2/2016

01-04-2016 | Original Paper

Altered Lamin A/C splice variant expression as a possible diagnostic marker in breast cancer

Authors: Ahmad Aljada, Joseph Doria, Ayman M. Saleh, Shahad H. Al-Matar, Sarah AlGabbani, Heba Bani Shamsa, Ahmad Al-Bawab, Altayeb Abdalla Ahmed

Published in: Cellular Oncology | Issue 2/2016

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Abstract

Background

Lamin A/C alternative splice variants (Lamin A, Lamin C, Lamin AΔ10 and Lamin AΔ50) have been implicated in cell cycle regulation, DNA replication, transcription regulation, cellular differentiation, apoptosis and aging. In addition, loss of Lamin A/C expression has been observed in several cancers, including breast cancer, and it has been found that Lamin A/C suppression may lead to cancer-like aberrations in nuclear morphology and aneuploidy. Based on these observations, we hypothesized that Lamin A/C transcript variant quantification might be employed for the diagnosis of breast cancer.

Methods

Newly designed TaqMan qRT-PCR assays for the analysis of Lamin A/C splice variants were validated and their use as biomarkers for the diagnosis of breast cancer was assessed using 16 normal breast tissues and 128 breast adenocarcinomas. In addition, the expression levels of the Lamin A/C transcript variants were measured in samples derived from seven other types of cancer.

Results

We found that the expression level of Lamin C was significantly increased in the breast tumors tested, whereas the expression levels of Lamin A and Lamin AΔ50 were significantly decreased. No significant change in Lamin AΔ10 expression was observed. Our data also indicated that the Lamin C : Lamin A mRNA ratio was increased in all clinical stages of breast cancer. Additionally, we observed increased Lamin C : Lamin A mRNA ratios in liver, lung and thyroid carcinomas and in colon, ovary and prostate adenocarcinomas.

Conclusions

From our data we conclude that the Lamin C : Lamin A mRNA ratio is increased in breast cancer and that this mRNA ratio may be of diagnostic use in all clinical stages of breast cancer and, possibly, also in liver, lung, thyroid, colon, ovary and prostate cancers.
Literature
1.
go back to reference J.L. Broers, B.M. Machiels, G.J. van Eys, H.J. Kuijpers, E.M. Manders, R. van Driel, F.C. Ramaekers, Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins. J. Cell Sci. 112(Pt 20), 3463–3475 (1999)PubMed J.L. Broers, B.M. Machiels, G.J. van Eys, H.J. Kuijpers, E.M. Manders, R. van Driel, F.C. Ramaekers, Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins. J. Cell Sci. 112(Pt 20), 3463–3475 (1999)PubMed
2.
go back to reference A. Taddei, F. Hediger, F.R. Neumann, S.M. Gasser, The function of nuclear architecture: a genetic approach. Annu. Rev. Genet. 38, 305–345 (2004)CrossRefPubMed A. Taddei, F. Hediger, F.R. Neumann, S.M. Gasser, The function of nuclear architecture: a genetic approach. Annu. Rev. Genet. 38, 305–345 (2004)CrossRefPubMed
4.
go back to reference H. Cao, R.A. Hegele, LMNA is mutated in Hutchinson-Gilford progeria (MIM 176670) but not in Wiedemann-Rautenstrauch progeroid syndrome (MIM 264090). J. Hum. Genet. 48, 271–274 (2003)CrossRefPubMed H. Cao, R.A. Hegele, LMNA is mutated in Hutchinson-Gilford progeria (MIM 176670) but not in Wiedemann-Rautenstrauch progeroid syndrome (MIM 264090). J. Hum. Genet. 48, 271–274 (2003)CrossRefPubMed
5.
go back to reference A. De Sandre-Giovannoli, R. Bernard, P. Cau, C. Navarro, J. Amiel, I. Boccaccio, S. Lyonnet, C.L. Stewart, A. Munnich, M. Le Merrer, N. Levy, Lamin a truncation in Hutchinson-Gilford progeria. Science 300, 2055 (2003)CrossRefPubMed A. De Sandre-Giovannoli, R. Bernard, P. Cau, C. Navarro, J. Amiel, I. Boccaccio, S. Lyonnet, C.L. Stewart, A. Munnich, M. Le Merrer, N. Levy, Lamin a truncation in Hutchinson-Gilford progeria. Science 300, 2055 (2003)CrossRefPubMed
6.
go back to reference M. Eriksson, W.T. Brown, L.B. Gordon, M.W. Glynn, J. Singer, L. Scott, M.R. Erdos, C.M. Robbins, T.Y. Moses, P. Berglund, A. Dutra, E. Pak, S. Durkin, A.B. Csoka, M. Boehnke, T.W. Glover, F.S. Collins, Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423, 293–298 (2003)CrossRefPubMed M. Eriksson, W.T. Brown, L.B. Gordon, M.W. Glynn, J. Singer, L. Scott, M.R. Erdos, C.M. Robbins, T.Y. Moses, P. Berglund, A. Dutra, E. Pak, S. Durkin, A.B. Csoka, M. Boehnke, T.W. Glover, F.S. Collins, Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423, 293–298 (2003)CrossRefPubMed
7.
go back to reference B.M. Machiels, A.H. Zorenc, J.M. Endert, H.J. Kuijpers, G.J. van Eys, F.C. Ramaekers, J.L. Broers, An alternative splicing product of the lamin A/C gene lacks exon 10. J. Biol. Chem. 271, 9249–9253 (1996)CrossRefPubMed B.M. Machiels, A.H. Zorenc, J.M. Endert, H.J. Kuijpers, G.J. van Eys, F.C. Ramaekers, J.L. Broers, An alternative splicing product of the lamin A/C gene lacks exon 10. J. Biol. Chem. 271, 9249–9253 (1996)CrossRefPubMed
8.
go back to reference L. Mounkes, S. Kozlov, B. Burke, C.L. Stewart, The laminopathies: nuclear structure meets disease. Curr. Opin. Genet. Dev. 13, 223–230 (2003)CrossRefPubMed L. Mounkes, S. Kozlov, B. Burke, C.L. Stewart, The laminopathies: nuclear structure meets disease. Curr. Opin. Genet. Dev. 13, 223–230 (2003)CrossRefPubMed
9.
go back to reference A. Muchir, H.J. Worman, The nuclear envelope and human disease. Physiology (Bethesda) 19, 309–314 (2004)CrossRef A. Muchir, H.J. Worman, The nuclear envelope and human disease. Physiology (Bethesda) 19, 309–314 (2004)CrossRef
10.
go back to reference D. McClintock, D. Ratner, M. Lokuge, D.M. Owens, L.B. Gordon, F.S. Collins, K. Djabali, The mutant form of lamin A that causes Hutchinson-Gilford progeria is a biomarker of cellular aging in human skin. PLoS One 2, e1269 (2007)CrossRefPubMedPubMedCentral D. McClintock, D. Ratner, M. Lokuge, D.M. Owens, L.B. Gordon, F.S. Collins, K. Djabali, The mutant form of lamin A that causes Hutchinson-Gilford progeria is a biomarker of cellular aging in human skin. PLoS One 2, e1269 (2007)CrossRefPubMedPubMedCentral
11.
go back to reference B.C. Capell, F.S. Collins, Human laminopathies: nuclei gone genetically awry. Nat. Rev. Genet. 7, 940–952 (2006)CrossRefPubMed B.C. Capell, F.S. Collins, Human laminopathies: nuclei gone genetically awry. Nat. Rev. Genet. 7, 940–952 (2006)CrossRefPubMed
12.
13.
go back to reference C.D. Capo-chichi, K.Q. Cai, J. Smedberg, P. Ganjei-Azar, A.K. Godwin, X.X. Xu, Loss of A-type lamin expression compromises nuclear envelope integrity in breast cancer. Chin. J. Cancer 30, 415–425 (2011)CrossRefPubMedPubMedCentral C.D. Capo-chichi, K.Q. Cai, J. Smedberg, P. Ganjei-Azar, A.K. Godwin, X.X. Xu, Loss of A-type lamin expression compromises nuclear envelope integrity in breast cancer. Chin. J. Cancer 30, 415–425 (2011)CrossRefPubMedPubMedCentral
14.
go back to reference B.M. Machiels, J.L. Broers, Y. Raymond, L. de Ley, H.J. Kuijpers, N.E. Caberg, F.C. Ramaekers, Abnormal A-type lamin organization in a human lung carcinoma cell line. Eur. J. Cell Biol. 67, 328–335 (1995)PubMed B.M. Machiels, J.L. Broers, Y. Raymond, L. de Ley, H.J. Kuijpers, N.E. Caberg, F.C. Ramaekers, Abnormal A-type lamin organization in a human lung carcinoma cell line. Eur. J. Cell Biol. 67, 328–335 (1995)PubMed
15.
go back to reference C.D. Capo-chichi, B. Aguida, N.W. Chabi, Q.K. Cai, G. Offrin, V.K. Agossou, A. Sanni, X.-X. Xu, Lamin A/C deficiency is an independent risk factor for cervical cancer. Cell. Oncol. (2015). doi:10.1007/s13402-015-0252-6 C.D. Capo-chichi, B. Aguida, N.W. Chabi, Q.K. Cai, G. Offrin, V.K. Agossou, A. Sanni, X.-X. Xu, Lamin A/C deficiency is an independent risk factor for cervical cancer. Cell. Oncol. (2015). doi:10.​1007/​s13402-015-0252-6
16.
go back to reference B. Stadelmann, E. Khandjian, A. Hirt, A. Luthy, R. Weil, H.P. Wagner, Repression of nuclear lamin A and C gene expression in human acute lymphoblastic leukemia and non-Hodgkin’s lymphoma cells. Leuk. Res. 14, 815–821 (1990)CrossRefPubMed B. Stadelmann, E. Khandjian, A. Hirt, A. Luthy, R. Weil, H.P. Wagner, Repression of nuclear lamin A and C gene expression in human acute lymphoblastic leukemia and non-Hodgkin’s lymphoma cells. Leuk. Res. 14, 815–821 (1990)CrossRefPubMed
17.
go back to reference R. Agrelo, F. Setien, J. Espada, M.J. Artiga, M. Rodriguez, A. Perez-Rosado, A. Sanchez-Aguilera, M.F. Fraga, M.A. Piris, M. Esteller, Inactivation of the lamin A/C gene by CpG island promoter hypermethylation in hematologic malignancies, and its association with poor survival in nodal diffuse large B-cell lymphoma. J. Clin. Oncol. 23, 3940–3947 (2005)CrossRefPubMed R. Agrelo, F. Setien, J. Espada, M.J. Artiga, M. Rodriguez, A. Perez-Rosado, A. Sanchez-Aguilera, M.F. Fraga, M.A. Piris, M. Esteller, Inactivation of the lamin A/C gene by CpG island promoter hypermethylation in hematologic malignancies, and its association with poor survival in nodal diffuse large B-cell lymphoma. J. Clin. Oncol. 23, 3940–3947 (2005)CrossRefPubMed
18.
go back to reference J.D. Debes, T.J. Sebo, H.V. Heemers, B.R. Kipp, D.L. Haugen, C.M. Lohse, D.J. Tindall, p300 modulates nuclear morphology in prostate cancer. Cancer Res. 65, 708–712 (2005)CrossRefPubMed J.D. Debes, T.J. Sebo, H.V. Heemers, B.R. Kipp, D.L. Haugen, C.M. Lohse, D.J. Tindall, p300 modulates nuclear morphology in prostate cancer. Cancer Res. 65, 708–712 (2005)CrossRefPubMed
19.
go back to reference L. Kong, G. Schafer, H. Bu, Y. Zhang, H. Klocker, Lamin A/C protein is overexpressed in tissue-invading prostate cancer and promotes prostate cancer cell growth, migration and invasion through the PI3K/AKT/PTEN pathway. Carcinogenesis 33, 751–759 (2012)CrossRefPubMed L. Kong, G. Schafer, H. Bu, Y. Zhang, H. Klocker, Lamin A/C protein is overexpressed in tissue-invading prostate cancer and promotes prostate cancer cell growth, migration and invasion through the PI3K/AKT/PTEN pathway. Carcinogenesis 33, 751–759 (2012)CrossRefPubMed
20.
go back to reference N.D. Willis, T.R. Cox, S.F. Rahman-Casans, K. Smits, S.A. Przyborski, P. van den Brandt, M. van Engeland, M. Weijenberg, R.G. Wilson, A. de Bruine, C.J. Hutchison, Lamin A/C is a risk biomarker in colorectal cancer. PLoS One 3, e2988 (2008)CrossRefPubMedPubMedCentral N.D. Willis, T.R. Cox, S.F. Rahman-Casans, K. Smits, S.A. Przyborski, P. van den Brandt, M. van Engeland, M. Weijenberg, R.G. Wilson, A. de Bruine, C.J. Hutchison, Lamin A/C is a risk biomarker in colorectal cancer. PLoS One 3, e2988 (2008)CrossRefPubMedPubMedCentral
21.
go back to reference N.D. Willis, R.G. Wilson, C.J. Hutchison, Lamin A: a putative colonic epithelial stem cell biomarker which identifies colorectal tumours with a more aggressive phenotype. Biochem. Soc. Trans. 36, 1350–1353 (2008)CrossRefPubMed N.D. Willis, R.G. Wilson, C.J. Hutchison, Lamin A: a putative colonic epithelial stem cell biomarker which identifies colorectal tumours with a more aggressive phenotype. Biochem. Soc. Trans. 36, 1350–1353 (2008)CrossRefPubMed
22.
go back to reference E.J. Belt, R.J. Fijneman, E.G. van den Berg, H. Bril, P.M. Delis-van Diemen, M. Tijssen, H.F. van Essen, E.S. de Lange-de Klerk, J.A. Belien, H.B. Stockmann, S. Meijer, G.A. Meijer, Loss of lamin A/C expression in stage II and III colon cancer is associated with disease recurrence. Eur. J. Cancer 47, 1837–1845 (2011)CrossRefPubMed E.J. Belt, R.J. Fijneman, E.G. van den Berg, H. Bril, P.M. Delis-van Diemen, M. Tijssen, H.F. van Essen, E.S. de Lange-de Klerk, J.A. Belien, H.B. Stockmann, S. Meijer, G.A. Meijer, Loss of lamin A/C expression in stage II and III colon cancer is associated with disease recurrence. Eur. J. Cancer 47, 1837–1845 (2011)CrossRefPubMed
23.
go back to reference P. Scaffidi, T. Misteli, Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat. Med. 11, 440–445 (2005)CrossRefPubMedPubMedCentral P. Scaffidi, T. Misteli, Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat. Med. 11, 440–445 (2005)CrossRefPubMedPubMedCentral
24.
go back to reference S. Rodriguez, F. Coppede, H. Sagelius, M. Eriksson, Increased expression of the Hutchinson-Gilford progeria syndrome truncated lamin A transcript during cell aging. Eur. J. Hum. Genet. 17, 928–937 (2009)CrossRefPubMedPubMedCentral S. Rodriguez, F. Coppede, H. Sagelius, M. Eriksson, Increased expression of the Hutchinson-Gilford progeria syndrome truncated lamin A transcript during cell aging. Eur. J. Hum. Genet. 17, 928–937 (2009)CrossRefPubMedPubMedCentral
25.
go back to reference J.I. Toth, S.H. Yang, X. Qiao, A.P. Beigneux, M.H. Gelb, C.L. Moulson, J.H. Miner, S.G. Young, L.G. Fong, Blocking protein farnesyltransferase improves nuclear shape in fibroblasts from humans with progeroid syndromes. Proc. Natl. Acad. Sci. U. S. A. 102, 12873–12878 (2005)CrossRefPubMedPubMedCentral J.I. Toth, S.H. Yang, X. Qiao, A.P. Beigneux, M.H. Gelb, C.L. Moulson, J.H. Miner, S.G. Young, L.G. Fong, Blocking protein farnesyltransferase improves nuclear shape in fibroblasts from humans with progeroid syndromes. Proc. Natl. Acad. Sci. U. S. A. 102, 12873–12878 (2005)CrossRefPubMedPubMedCentral
26.
go back to reference C.L. Moulson, L.G. Fong, J.M. Gardner, E.A. Farber, G. Go, A. Passariello, D.K. Grange, S.G. Young, J.H. Miner, Increased progerin expression associated with unusual LMNA mutations causes severe progeroid syndromes. Hum. Mutat. 28, 882–889 (2007)CrossRefPubMed C.L. Moulson, L.G. Fong, J.M. Gardner, E.A. Farber, G. Go, A. Passariello, D.K. Grange, S.G. Young, J.H. Miner, Increased progerin expression associated with unusual LMNA mutations causes severe progeroid syndromes. Hum. Mutat. 28, 882–889 (2007)CrossRefPubMed
27.
28.
go back to reference I.C. Lopez-Mejia, M. de Toledo, C. Chavey, L. Lapasset, P. Cavelier, C. Lopez-Herrera, K. Chebli, P. Fort, G. Beranger, L. Fajas, E.Z. Amri, F. Casas, J. Tazi, Antagonistic functions of LMNA isoforms in energy expenditure and lifespan. EMBO Rep. 15, 529–539 (2014)CrossRefPubMedPubMedCentral I.C. Lopez-Mejia, M. de Toledo, C. Chavey, L. Lapasset, P. Cavelier, C. Lopez-Herrera, K. Chebli, P. Fort, G. Beranger, L. Fajas, E.Z. Amri, F. Casas, J. Tazi, Antagonistic functions of LMNA isoforms in energy expenditure and lifespan. EMBO Rep. 15, 529–539 (2014)CrossRefPubMedPubMedCentral
29.
go back to reference J.L. Broers, B.M. Machiels, H.J. Kuijpers, F. Smedts, R. van den Kieboom, Y. Raymond, F.C. Ramaekers, A- and B-type lamins are differentially expressed in normal human tissues. Histochem. Cell Biol. 107, 505–517 (1997)CrossRefPubMed J.L. Broers, B.M. Machiels, H.J. Kuijpers, F. Smedts, R. van den Kieboom, Y. Raymond, F.C. Ramaekers, A- and B-type lamins are differentially expressed in normal human tissues. Histochem. Cell Biol. 107, 505–517 (1997)CrossRefPubMed
30.
go back to reference M.A. Eckersley-Maslin, J.H. Bergmann, Z. Lazar, D.L. Spector, Lamin A/C is expressed in pluripotent mouse embryonic stem cells. Nucleus 4, 53–60 (2013)CrossRefPubMedPubMedCentral M.A. Eckersley-Maslin, J.H. Bergmann, Z. Lazar, D.L. Spector, Lamin A/C is expressed in pluripotent mouse embryonic stem cells. Nucleus 4, 53–60 (2013)CrossRefPubMedPubMedCentral
31.
go back to reference R.A. Rober, K. Weber, M. Osborn, Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 105, 365–378 (1989)PubMed R.A. Rober, K. Weber, M. Osborn, Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 105, 365–378 (1989)PubMed
32.
go back to reference J. Swift, I.L. Ivanovska, A. Buxboim, T. Harada, P.C. Dingal, J. Pinter, J.D. Pajerowski, K.R. Spinler, J.W. Shin, M. Tewari, F. Rehfeldt, D.W. Speicher, D.E. Discher, Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104 (2013)CrossRefPubMedPubMedCentral J. Swift, I.L. Ivanovska, A. Buxboim, T. Harada, P.C. Dingal, J. Pinter, J.D. Pajerowski, K.R. Spinler, J.W. Shin, M. Tewari, F. Rehfeldt, D.W. Speicher, D.E. Discher, Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104 (2013)CrossRefPubMedPubMedCentral
33.
go back to reference H.J. Jung, J.M. Lee, S.H. Yang, S.G. Young, L.G. Fong, Nuclear lamins in the brain - new insights into function and regulation. Mol. Neurobiol. 47, 290–301 (2013)CrossRefPubMedPubMedCentral H.J. Jung, J.M. Lee, S.H. Yang, S.G. Young, L.G. Fong, Nuclear lamins in the brain - new insights into function and regulation. Mol. Neurobiol. 47, 290–301 (2013)CrossRefPubMedPubMedCentral
34.
go back to reference T. Wakabayashi, T. Mori, Y. Hirahara, T. Koike, Y. Kubota, Y. Takamori, H. Yamada, Nuclear lamins are differentially expressed in retinal neurons of the adult rat retina. Histochem. Cell Biol. 136, 427–436 (2011)CrossRefPubMed T. Wakabayashi, T. Mori, Y. Hirahara, T. Koike, Y. Kubota, Y. Takamori, H. Yamada, Nuclear lamins are differentially expressed in retinal neurons of the adult rat retina. Histochem. Cell Biol. 136, 427–436 (2011)CrossRefPubMed
35.
go back to reference C.J. Hutchison, H.J. Worman, A-type lamins: guardians of the soma? Nat. Cell Biol. 6, 1062–1067 (2004)CrossRefPubMed C.J. Hutchison, H.J. Worman, A-type lamins: guardians of the soma? Nat. Cell Biol. 6, 1062–1067 (2004)CrossRefPubMed
36.
go back to reference F. Lin, H.J. Worman, Expression of nuclear lamins in human tissues and cancer cell lines and transcription from the promoters of the lamin A/C and B1 genes. Exp. Cell Res. 236, 378–384 (1997)CrossRefPubMed F. Lin, H.J. Worman, Expression of nuclear lamins in human tissues and cancer cell lines and transcription from the promoters of the lamin A/C and B1 genes. Exp. Cell Res. 236, 378–384 (1997)CrossRefPubMed
37.
go back to reference A. Matsumoto, M. Hieda, Y. Yokoyama, Y. Nishioka, K. Yoshidome, M. Tsujimoto, N. Matsuura, Global loss of a nuclear lamina component, lamin A/C, and LINC complex components SUN1, SUN2, and nesprin-2 in breast cancer. Canc. Med. 4, 1547–1557 (2015)CrossRef A. Matsumoto, M. Hieda, Y. Yokoyama, Y. Nishioka, K. Yoshidome, M. Tsujimoto, N. Matsuura, Global loss of a nuclear lamina component, lamin A/C, and LINC complex components SUN1, SUN2, and nesprin-2 in breast cancer. Canc. Med. 4, 1547–1557 (2015)CrossRef
38.
go back to reference U. Wazir, M.H. Ahmed, J.M. Bridger, A. Harvey, W.G. Jiang, A.K. Sharma, K. Mokbel, The clinicopathological significance of lamin A/C, lamin B1 and lamin B receptor mRNA expression in human breast cancer. Cell. Mol. Biol. Lett. 18, 595–611 (2013)CrossRefPubMed U. Wazir, M.H. Ahmed, J.M. Bridger, A. Harvey, W.G. Jiang, A.K. Sharma, K. Mokbel, The clinicopathological significance of lamin A/C, lamin B1 and lamin B receptor mRNA expression in human breast cancer. Cell. Mol. Biol. Lett. 18, 595–611 (2013)CrossRefPubMed
39.
go back to reference W.S. Lee, J.J. Jung, H.C. Jeung, S.W. Noh, B.K. Oh, K.Y. Kim, T.S. Kim, H.C. Chung, J.K. Roh, S.Y. Rha, Methylation status of lamin A/C in gastric cancer cell lines. Hepatogastroenterology 59, 1313–1318 (2012)CrossRefPubMed W.S. Lee, J.J. Jung, H.C. Jeung, S.W. Noh, B.K. Oh, K.Y. Kim, T.S. Kim, H.C. Chung, J.K. Roh, S.Y. Rha, Methylation status of lamin A/C in gastric cancer cell lines. Hepatogastroenterology 59, 1313–1318 (2012)CrossRefPubMed
40.
go back to reference D. Constantinescu, H.L. Gray, P.J. Sammak, G.P. Schatten, A.B. Csoka, Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24, 177–185 (2006)CrossRefPubMed D. Constantinescu, H.L. Gray, P.J. Sammak, G.P. Schatten, A.B. Csoka, Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24, 177–185 (2006)CrossRefPubMed
41.
go back to reference D. Lourim, J.J. Lin, Expression of nuclear lamin A and muscle-specific proteins in differentiating muscle cells in ovo and in vitro. J. Cell Biol. 109, 495–504 (1989)CrossRefPubMed D. Lourim, J.J. Lin, Expression of nuclear lamin A and muscle-specific proteins in differentiating muscle cells in ovo and in vitro. J. Cell Biol. 109, 495–504 (1989)CrossRefPubMed
42.
go back to reference B. Liu, J. Wang, K.M. Chan, W.M. Tjia, W. Deng, X. Guan, J.D. Huang, K.M. Li, P.Y. Chau, D.J. Chen, D. Pei, A.M. Pendas, J. Cadinanos, C. Lopez-Otin, H.F. Tse, C. Hutchison, J. Chen, Y. Cao, K.S. Cheah, K. Tryggvason, Z. Zhou, Genomic instability in laminopathy-based premature aging. Nat. Med. 11, 780–785 (2005)CrossRefPubMed B. Liu, J. Wang, K.M. Chan, W.M. Tjia, W. Deng, X. Guan, J.D. Huang, K.M. Li, P.Y. Chau, D.J. Chen, D. Pei, A.M. Pendas, J. Cadinanos, C. Lopez-Otin, H.F. Tse, C. Hutchison, J. Chen, Y. Cao, K.S. Cheah, K. Tryggvason, Z. Zhou, Genomic instability in laminopathy-based premature aging. Nat. Med. 11, 780–785 (2005)CrossRefPubMed
43.
go back to reference A. Peter, R. Stick, Evolution of the lamin protein family: what introns can tell. Nucleus 3, 44–59 (2012)CrossRefPubMed A. Peter, R. Stick, Evolution of the lamin protein family: what introns can tell. Nucleus 3, 44–59 (2012)CrossRefPubMed
44.
go back to reference Y.S. Oh, D.G. Kim, G. Kim, E.C. Choi, B.K. Kennedy, Y. Suh, B.J. Park, S. Kim, Downregulation of lamin A by tumor suppressor AIMP3/p18 leads to a progeroid phenotype in mice. Aging Cell 9, 810–822 (2010)CrossRefPubMed Y.S. Oh, D.G. Kim, G. Kim, E.C. Choi, B.K. Kennedy, Y. Suh, B.J. Park, S. Kim, Downregulation of lamin A by tumor suppressor AIMP3/p18 leads to a progeroid phenotype in mice. Aging Cell 9, 810–822 (2010)CrossRefPubMed
Metadata
Title
Altered Lamin A/C splice variant expression as a possible diagnostic marker in breast cancer
Authors
Ahmad Aljada
Joseph Doria
Ayman M. Saleh
Shahad H. Al-Matar
Sarah AlGabbani
Heba Bani Shamsa
Ahmad Al-Bawab
Altayeb Abdalla Ahmed
Publication date
01-04-2016
Publisher
Springer Netherlands
Published in
Cellular Oncology / Issue 2/2016
Print ISSN: 2211-3428
Electronic ISSN: 2211-3436
DOI
https://doi.org/10.1007/s13402-015-0265-1

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