Laminin-332-rich tumor microenvironment for tumor invasion in the interface zone of breast cancer
Open accessAbstract
Dense fibrosis, which is caused by desmoplastic reaction, is usually found in invasive ductal carcinoma and may represent the alteration of the tumor microenvironment preceding tumor invasion. Thus, the dense fibrotic zone around invasive ductal carcinoma can be considered to be the actual tissue site of tumor microenvironment, where the precedent alterations for tumor invasion occur. To characterize the dense fibrotic zone, we classified invasive ductal carcinoma tissue into a tumor zone, a normal zone, and the novel interface zone (IZ), which shows dense fibrosis. The postulated IZ is a 5-mm-wide belt that circles the tumor margin and overlaps with normal tissue. Of the extracellular matrix components, laminin-332 was specifically overexpressed in the IZ. Events that appear to be similar to the epithelial-mesenchymal transition, a novel source of myofibroblast formation from epithelial cells, were observed in the IZ, according to the following characteristics: overexpression of matrix metalloproteinase 3, membrane type 1-matrix metalloproteinase, snail, and zinc finger E-box-binding homeobox 1, and the gain of N-cadherin expression, as well as the down-regulation of miR200c. The myofibroblasts isolated from the IZ, which were designated interface zone-fibroblast, displayed laminin-332 and membrane type 1-matrix metalloproteinase overexpression, in contrast with both cancer-associated fibroblasts and normal breast fibroblasts. Taken together, our results suggest that the IZ, which shows dense fibrosis, may provide a specialized microenvironment for guiding tumor invasion: the fibrosis caused by laminin-332 overexpressing myofibroblast formation (interface zone-fibroblast) via epithelial-mesenchymal transition.
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The extracellular matrix (ECM) is a highly dynamic and structurally complex scaffold that plays a critical role in regulating tumor progression and therapeutic response.
“The extracellular matrix (ECM), a non-cellular component of the TME, is a highly dynamic and structurally complex scaffold that plays a critical role in regulating tumor progression and therapeutic response [72,73,74].”
From Modeling Tumor Microenvironment Complexity In Vitro: Spheroids as Physiologically Relevant Tumor Models and Strategies for Their Analysis (2025) · cites this paper as [73]
The Discussion (page not supplied) calls the ECM a major component of the tumor microenvironment and reports ECM changes associated with tumor progression. The paper also describes a role for the ECM component laminin-332 in tumor-cell invasion, but it does not establish that ECM regulates therapeutic response. Its suggestion that the interface zone could be a treatment target is not evidence about treatment response. (LLM, conf=0.86)
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Cites
The Versatile Role of microRNA-30a in Human Cancer
Wang, C., Yang, X., Chen, Y., & Chen, L. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000471111 · Cited by 3,409 · see citing works
Epithelial-mesenchymal transition and its implications for fibrosis
Kalluri, R., & Neilson, E. G. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20530 · Cited by 2,651 · see citing works
The microenvironment of the tumour–host interface
Liotta, L. A., & Kohn, E. C. (2001) · Nature · doi:10.1038/35077241 · Cited by 2,322 · see citing works
Bissell, M. J., & Radisky, D. (2001) · Nature Reviews Cancer · doi:10.1038/35094059 · Cited by 2,180 · see citing works
Integrin signalling during tumour progression
Guo, W., & Giancotti, F. G. (2004) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1490 · Cited by 1,473 · see citing works
Carcinoma-associated fibroblasts stimulate tumor progression of initiated human epithelium
Olumi, A., Grossfeld, G., Hayward, S., Carroll, P., Cunha, G., Hein, P., & Tlsty, T. (2000) · Breast Cancer Research · doi:10.1186/bcr138 · Cited by 1,463 · see citing works
Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability
Radisky, D. C., Levy, D. D., Littlepage, L. E., Liu, H., Nelson, C. M., Fata, J. E., Leake, D., Godden, E. L., Albertson, D. G., Angela Nieto, M., et al. (2005) · Nature · doi:10.1038/nature03688 · Cited by 1,284 · see citing works
Identification and characterization of a fibroblast marker: FSP1.
Strutz, F. M., Okada, H., Lo, C. W., Danoff, T. M., Carone, R. L., Tomaszewski, J. E., & Neilson, E. G. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.130.2.393 · Cited by 1,075 · see citing works
Rhyu, D. Y., Yang, Y., Ha, H., Lee, G. T., Song, J. S., Uh, S., & Lee, H. B. (2005) · Journal of the American Society of Nephrology · doi:10.1681/asn.2004050425 · Cited by 523 · see citing works
Ng, Y.-Y., Huang, T., Yang, W.-C., Chen, Z.-P., Yang, A., Mu, W., Nikolic‐Paterson, D. J., Atkins, R. C., & Lan, H. Y. (1998) · Kidney International · doi:10.1046/j.1523-1755.1998.00076.x · Cited by 396 · see citing works
Hinz, B. (2009) · Current Rheumatology Reports · doi:10.1007/s11926-009-0017-1 · Cited by 373 · see citing works
Fibrosis and cancer: Do myofibroblasts come also from epithelial cells via EMT?
Radisky, D. C., Kenny, P. A., & Bissell, M. J. (2007) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21186 · Cited by 342 · see citing works
Laminin 332 in squamous-cell carcinoma
Marinkovich, M. P. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2089 · Cited by 299 · see citing works
Flier, S. N., Tanjore, H., Kokkotou, E. G., Sugimoto, H., Zeisberg, M., & Kalluri, R. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.102012 · Cited by 282 · see citing works
Giannelli, G., Bergamini, C., Fransvea, E., Sgarra, C., & Antonaci, S. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.09.055 · Cited by 251 · see citing works
Weaver, V. M., Bissell, M. J., Fischer, A. H., & Peterson, O. W. (1996) · Biochemistry and Cell Biology · doi:10.1139/o96-089 · Cited by 212 · see citing works
Current Perceptions Regarding Surgical Margin Status After Breast-Conserving Therapy
Taghian, A. G., Mohiuddin, M. M., Jagsi, R., Goldberg, S. I., Ceilley, E., & Powell, S. N. (2005) · Annals of Surgery · doi:10.1097/01.sla.0000157272.04803.1b · Cited by 209 · see citing works
Laminin‐5 (laminin‐332): Unique biological activity and role in tumor growth and invasion
Miyazaki, K. (2006) · Cancer Science · doi:10.1111/j.1349-7006.2006.00150.x · Cited by 198 · see citing works
Pullar, C. E., Baier, B. S., Kariya, Y., Russell, A. J., Horst, B. A. J., Marinkovich, M. P., & Isseroff, R. R. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-05-0433 · Cited by 144 · see citing works
Munshi, H. G., Wu, Y., Mukhopadhyay, S., Ottaviano, A. J., Sassano, A., Koblinski, J. E., Platanias, L. C., & Stack, M. S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404958200 · Cited by 137 · see citing works
Ha, H. Y., Moon, H. B., Nam, M. S., Lee, J., Ryoo, Z. Y., Lee, T., Lee, K. K., So, B. J., Sato, H., Seiki, M., et al. (2001) · PubMed · Cited by 137 · see citing works
Origin and function of tumor stroma fibroblasts
Xouri, G., & Christian, S. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.11.017 · Cited by 116 · see citing works
Cao, J. P., Chiarelli, C., Richman, O., Zarrabi, K. K., Kozarekar, P., & Zucker, S. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m705759200 · Cited by 106 · see citing works
Giannelli, G., Fransvea, E., Bergamini, C., Marinosci, F., & Antonaci, S. (2003) · PubMed · Cited by 97 · see citing works
Mizushima, H., Miyagi, Y., Kikkawa, Y., Yamanaka, N., Yasumitsu, H., Misugi, K., & Miyazaki, K. (1996) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a021541 · Cited by 97 · see citing works
Fibroblast-derived MT1-MMP promotes tumor progression in vitro and in vivo
Zhang, W., Matrisian, L. M., Holmbeck, K., Vick, C. C., & Rosenthal, E. L. (2006) · BMC Cancer · doi:10.1186/1471-2407-6-52 · Cited by 95 · see citing works
Down-Regulation of Laminin-5 in Breast Carcinoma Cells
Martin, K. J., Kwan, C., Nagasaki, K., Zhang, X., O’Hare, M. J., Kaelin, C. M., Burgeson, R. E., Pardee, A. B., & Sager, R. (1998) · Molecular Medicine · doi:10.1007/bf03401760 · Cited by 85 · see citing works
Potential mRNA Degradation Targets of hsa-miR-200c
Hurteau, G. J., Spivack, S. D., & Brock, G. (2006) · Cell Cycle · doi:10.4161/cc.5.17.3133 · Cited by 81 · see citing works
Investigation into the Mechanism of the Loss of Laminin 5 (α3β3γ2) Expression in Prostate Cancer
Hao, J., Jackson, L., Calaluce, R., McDaniel, K. M., Dalkin, B. L., & Nagle, R. B. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64060-6 · Cited by 81 · see citing works
Montel, V., Mose, E. S., & Tarin, D. (2006) · International Journal of Cancer · doi:10.1002/ijc.21757 · Cited by 63 · see citing works
Motility Induction in Breast Carcinoma by Mammary Epithelial Laminin 332 (Laminin 5)
Carpenter, P. M., Dao, A. V., Arain, Z. S., Chang, M. K. X., Nguyen, H. P. A., Arain, S., Wang‐Rodriguez, J., Kwon, S. Y., & Wilczynski, S. P. (2009) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-08-0148 · Cited by 59 · see citing works
Matrix Metalloproteinase–induced Fibrosis and Malignancy in Breast and Lung
Radisky, D. C., & Przybylo, J. A. (2008) · Proceedings of the American Thoracic Society · doi:10.1513/pats.200711-166dr · Cited by 47 · see citing works
Berndt, A., Hyckel, P., Könneker, A., Katenkamp, D., & Kosmehl, H. (1997) · PubMed · Cited by 47 · see citing works
Laminin 5 Expression in Metaplastic Breast Carcinomas
Carpenter, P. M., Wang‐Rodriguez, J., Chan, O. T. M., & Wilczynski, S. P. (2008) · The American Journal of Surgical Pathology · doi:10.1097/pas.0b013e3181592201 · Cited by 44 · see citing works
Flagged first, then by citations
3 of the 37 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The extracellular matrix in tumor progression and metastasis
Eble, J. A., & Niland, S. (2019) · Clinical & Experimental Metastasis · doi:10.1007/s10585-019-09966-1 · Cited by 613 · see citing works
The extracellular matrix in breast cancer
Insua-Rodríguez, J., & Oskarsson, T. (2016) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.12.017 · Cited by 470 · see citing works
Interstitial guidance of cancer invasion
Gritsenko, P. G., Ilina, O., & Friedl, P. (2011) · The Journal of Pathology · doi:10.1002/path.3031 · Cited by 347 · see citing works
Host Matrix Modulation by Tumor Exosomes Promotes Motility and Invasiveness
Mu, W., Rana, S., & Zöller, M. (2013) · Neoplasia · doi:10.1593/neo.13786 · Cited by 248 · see citing works
ITGB4-mediated metabolic reprogramming of cancer-associated fibroblasts
Sung, J. S., Kang, C. W., Kang, S., Jang, Y., Chae, Y. C., Kim, B. G., & Cho, N. H. (2019) · Oncogene · doi:10.1038/s41388-019-1014-0 · Cited by 171 · see citing works
Self-citationRousselle, P., & Scoazec, J. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.09.026 · Cited by 162 · see citing works
Evaluation of an Internet addiction treatment program for Chinese adolescents in Hong Kong.
Shek, D. T. L., Tang, V. M. Y., & Lo, C.-P. (2009) · PubMed · Cited by 135 · see citing works
Biofabrication methods for reconstructing extracellular matrix mimetics
Aazmi, A., Zhang, D., Mazzaglia, C., Yu, M., Wang, Z., Yang, H., Huang, Y. Y. S., & Ma, L. (2023) · Bioactive Materials · doi:10.1016/j.bioactmat.2023.08.018 · Cited by 138 · see citing works
Function of cancer cell-derived extracellular matrix in tumor progression
Xiong, G., & Xu, R. (2016) · Journal of Cancer Metastasis and Treatment · doi:10.20517/2394-4722.2016.08 · Cited by 128 · see citing works
Extracellular Matrix Dynamics as an Emerging yet Understudied Hallmark of Aging and Longevity
Statzer, C., Park, J. Y. C., & Ewald, C. (2023) · Aging and Disease · doi:10.14336/ad.2022.1116 · Cited by 75 · see citing works
Pouliot, N., & Kusuma, N. (2013) · Cell Adhesion & Migration · doi:10.4161/cam.22125 · Cited by 90 · see citing works
Active Roles of Tumor Stroma in Breast Cancer Metastasis
Khamis, Z. I., Sahab, Z. J., & Sang, Q. A. (2012) · International Journal of Breast Cancer · doi:10.1155/2012/574025 · Cited by 86 · see citing works
Zhou, B., Gibson-Corley, K. N., Herndon, M. E., Sun, Y., Gustafson-Wagner, E. A., Teoh-Fitzgerald, M. L. T., Domann, F. E., Henry, M. D., & Stipp, C. S. (2013) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-13-0184 · Cited by 80 · see citing works
Kim, B. G., Gao, M., Kang, S., Choi, Y. P., Lee, J. H., Kim, J. E., Han, H. H., Mun, S. G., & Cho, N. H. (2017) · Cell Death and Disease · doi:10.1038/cddis.2017.73 · Cited by 80 · see citing works
Self-citationHold on or Cut? Integrin- and MMP-Mediated Cell–Matrix Interactions in the Tumor Microenvironment
Niland, S., & Eble, J. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010238 · Cited by 79 · see citing works
Kim, B. G., Sung, J. S., Jang, Y., Cha, Y. J., Kang, S., Han, H. H., Lee, J. H., & Cho, N. H. (2019) · Communications Biology · doi:10.1038/s42003-019-0553-9 · Cited by 75 · see citing works
Self-citationKim, J. E., Kim, B. G., Jang, Y., Kang, S., Lee, J. H., & Cho, N. H. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.10.039 · Cited by 74 · see citing works
Self-citationRomano, V., Belviso, I., Venuta, A., Ruocco, M. R., Masone, S., Aliotta, F., Fiume, G., Montagnani, S., Avagliano, A., & Arcucci, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22105283 · Cited by 73 · see citing works
Regulators and mechanisms of anoikis in triple-negative breast cancer (TNBC): A review
Tajbakhsh, A., Rivandi, M., Abedini, S., Pasdar, A., & Sahebkar, A. (2019) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2019.05.009 · Cited by 71 · see citing works
Shah, S., & D’Souza, G. G. M. (2025) · Cells · doi:10.3390/cells14100732 · Cited by 66 · see citing works
Kim, B. G., Gao, M., Choi, Y. P., Kang, S., Park, H. R., Kang, K. S., & Cho, N. H. (2012) · Breast Cancer Research · doi:10.1186/bcr3203 · Cited by 66 · see citing works
Self-citationMolecular portraits of intratumoral heterogeneity in human ovarian cancer
Choi, Y. P., Shim, H. S., Gao, M., Kang, S., & Cho, N. H. (2011) · Cancer Letters · doi:10.1016/j.canlet.2011.03.018 · Cited by 65 · see citing works
Self-citationVieira, A. F., Ribeiro, A. S., Dionísio, M. R., Sousa, B., Nobre, A. R., Albergaria, A., Santiago-Gómez, A., Mendes, N. M., Gerhard, R., Schmitt, F. C., et al. (2014) · Oncotarget · doi:10.18632/oncotarget.1459 · Cited by 60 · see citing works
White, M. J. V., Roife, D., & Gomer, R. H. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1500365 · Cited by 60 · see citing works
Cavaco, A. C. M., Rezaei, M., Caliandro, M. F., Lima, A. M., Stehling, M., Dhayat, S. A., Haier, J., Brakebusch, C., & Eble, J. A. (2018) · Cancers · doi:10.3390/cancers11010014 · Cited by 60 · see citing works
Júnior, H. M., Rocha, V. N., Leite, C. F., de Aguiar, M. C. F., Souza, P. E. A., & Horta, M. C. R. (2013) · Journal of Oral Pathology and Medicine · doi:10.1111/jop.12121 · Cited by 58 · see citing works
ADAM12 Produced by Tumor Cells Rather than Stromal Cells Accelerates Breast Tumor Progression
Fröhlich, C., Nehammer, C., Albrechtsen, R., Kronqvist, P., Kveiborg, M., Sehara‐Fujisawa, A., Mercurio, A. M., & Wewer, U. M. (2011) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-11-0100 · Cited by 56 · see citing works
Lorusso, G., Wyss, C. B., Kuonen, F., Vannini, N., Billottet, C., Duffey, N., Pineau, R., Lan, Q., Wirapati, P., Barras, D., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.aax8933 · Cited by 53 · see citing works
Davies, A. E., & Albeck, J. G. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00044 · Cited by 50 · see citing works
The biomimetic extracellular matrix: a therapeutic tool for breast cancer research
Tamayo-Angorrilla, M., de Andrés, J. L., Jiménez, G., & Marchal, J. A. (2021) · Translational research · doi:10.1016/j.trsl.2021.11.008 · Cited by 49 · see citing works
Lam, C. R. I., Tan, C., Teo, Z. Q., Tay, C. Y., Phua, T., Wu, Y., Cai, P., Tan, L. P., Chen, X., Zhu, P., et al. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.339 · Cited by 48 · see citing works
Role of secreted type I collagen derived from stromal cells in two breast cancer cell lines
Kim, S. H., Lee, H. Y., Jung, S. P., Kim, S., Lee, J. E., Nam, S. J., & Bae, J. W. (2014) · Oncology Letters · doi:10.3892/ol.2014.2199 · Cited by 49 · see citing works
Kang, S., Maeng, H., Kim, B. G., Qing, G. M., Choi, Y. P., Kim, H. Y., Kim, P. S., Kim, Y., Kim, Y. H., Choi, Y. D., et al. (2012) · Journal of Proteome Research · doi:10.1021/pr3003672 · Cited by 48 · see citing works
Self-citationCancer Mechanobiology: Microenvironmental Sensing and Metastasis
Lee, G., Han, S., Lee, J., Kim, H., & Kim, D. (2019) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b01230 · Cited by 46 · see citing works
Robertson, C. (2016) · Experimental Cell Research · doi:10.1016/j.yexcr.2015.11.009 · Cited by 45 · see citing works
In Vitro Modeling of the Tumor Microenvironment in Tumor Organoids
Devarasetty, M., Forsythe, S. D., Shelkey, E., & Söker, S. (2020) · Tissue Engineering and Regenerative Medicine · doi:10.1007/s13770-020-00258-4 · Cited by 43 · see citing works
Parte, S. C., Kaur, A. B., Nimmakayala, R. K., Ogunleye, A. O., Chirravuri, R., Vengoji, R., Leon, F., Nallasamy, P., Rauth, S., Alsafwani, Z. W., et al. (2023) · Gastroenterology · doi:10.1053/j.gastro.2023.12.018 · Cited by 41 · see citing works
Aspects of Collagen Changes in Breast Cancer
Luparello, C. (2013) · Journal of Carcinogenesis & Mutagenesis · doi:10.4172/2157-2518.s13-007 · Cited by 41 · see citing works
The role of laminins in cancer pathobiology: a comprehensive review
Nonnast, E., Mira, E., & Mañes, S. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-06079-0 · Cited by 40 · see citing works
Chen, J., Yu, H. J., Lin, M., Mehta, R. S., & Su, M. (2013) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2013.07.014 · Cited by 39 · see citing works
Targeting ILK and β4 integrin abrogates the invasive potential of ovarian cancer
Choi, Y. P., Kim, B. G., Gao, M., Kang, S., & Cho, N. H. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.09.114 · Cited by 34 · see citing works
Self-citationSiljamäki, E., Rappu, P., Riihilä, P., Nissinen, L. M., Kähäri, V., & Heino, J. (2019) · Matrix Biology · doi:10.1016/j.matbio.2019.09.001 · Cited by 35 · see citing works
Laminin 332 expression and prognosis in breast cancer
Carpenter, P. M., Ziogas, A., Markham, E., Cantillep, A., Yan, R., & Anton‐Culver, H. (2018) · Human Pathology · doi:10.1016/j.humpath.2018.08.003 · Cited by 31 · see citing works
Ribeiro, J. R., Gaudet, H. M., Khan, M., Schorl, C., James, N. E., Oliver, M. T., DiSilvestro, P., Moore, R. G., & Yano, N. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2017.00332 · Cited by 29 · see citing works
Strategic outline of interventions targeting extracellular matrix for promoting healthy longevity
Park, J. Y. C., King, A., Björk, V., English, B. W., Fedintsev, A., & Ewald, C. Y. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00060.2023 · Cited by 29 · see citing works
Migration of breast cancer cell lines in response to pulmonary laminin 332
Carpenter, P. M., Sivadas, P., Hua, S. S., Xiao, C., Gutierrez, A. B., Ngo, T., & Gershon, P. D. (2016) · Cancer Medicine · doi:10.1002/cam4.957 · Cited by 26 · see citing works
The Tumor Microenvironment: Focus on Extracellular Matrix
Rigoglio, N. N., Rabêlo, A. C. S., Borghesi, J., Matias, G. D. S. S., Fratini, P., Prazeres, P. H. D. M., Pimentel, C. M. M., Birbrair, A., & Miglino, M. A. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-40146-7_1 · Cited by 27 · see citing works
Hsu, H.-C., Liu, L., Wang, H.-Y., Hung, C., Lin, Y.-C., Ho, C., & Way, T. (2017) · PLoS ONE · doi:10.1371/journal.pone.0164661 · Cited by 23 · see citing works
Lee, M.-S., Kim, S., Kim, B. G., Won, C., Nam, S. H., Kang, S., Kim, H., Kang, M., Ryu, J., Song, H. E., et al. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2014.05.007 · Cited by 20 · see citing works
Self-citationSingle-cell RNA reveals a tumorigenic microenvironment in the interface zone of human breast tumors
Yang, W. Y., Xu, M., Xu, S., Guan, Q., Geng, S., Wang, J., Wei, W., Xu, H., Liu, Y., Meng, Y., et al. (2023) · Breast Cancer Research · doi:10.1186/s13058-023-01703-7 · Cited by 16 · see citing works
Self-citationKim, M. Y., Cho, N., Koo, H. R., Yun, B. L., Bae, M. S., Chie, E. K., & Moon, W. K. (2013) · Acta Radiologica · doi:10.1177/0284185113483676 · Cited by 16 · see citing works
Self-citationLee, M.-H., Wu, P.-H., Gilkes, D. M., Aifuwa, I., & Wirtz, D. (2015) · Oncotarget · doi:10.18632/oncotarget.4728 · Cited by 16 · see citing works
Terabayashi, T., Hanada, K., Motani, K., Kosako, H., Yamaoka, M., Kimura, T., & Ishizaki, T. (2018) · Genes to Cells · doi:10.1111/gtc.12584 · Cited by 14 · see citing works
Identification of key genes in osteosarcoma by meta‑analysis of gene expression microarray
Sun, J., Xu, H., Qi, M., Zhang, C., & Shi, J. (2019) · Molecular Medicine Reports · doi:10.3892/mmr.2019.10543 · Cited by 14 · see citing works
Prognostic significance of circulating laminin gamma2 for early-stage non-small-cell lung cancer
Yue, W., Yu, T., Ma, L., Zhang, L., Guo, Y., Gu, M., Wang, Z., Wang, Y., & Wang, Z. (2016) · OncoTargets and Therapy · doi:10.2147/ott.s105732 · Cited by 12 · see citing works
Migration speed of captured breast cancer subpopulations correlates with metastatic fitness
Desjardins‐Lecavalier, N., Annis, M. G., Nowakowski, A., Kiepas, A., Binan, L., Roy, J., Modica, G., Hébert, S., Kleinman, C. L., Siegel, P. M., et al. (2023) · Journal of Cell Science · doi:10.1242/jcs.260835 · Cited by 11 · see citing works
Roy, N. S., Kumari, M., Alam, K., Bhattacharya, A., Kaity, S., Kaur, K., Ravichandiran, V., & Roy, S. (2024) · Progress in Biomedical Engineering · doi:10.1088/2516-1091/ad9dcb · Cited by 10 · see citing works
Inhibition of TGF-β signaling, invasion, and growth of cutaneous squamous cell carcinoma by PLX8394
Siljamäki, E., Riihilä, P., Suwal, U., Nissinen, L. M., Rappu, P., Kallajoki, M. A., Kähäri, V., & Heino, J. (2023) · Oncogene · doi:10.1038/s41388-023-02863-8 · Cited by 10 · see citing works
Transcriptome Analysis of Liver Cancer Cell Huh-7 Treated With Metformin
Li, C., Liu, Z., Liu, S., Zhang, G.-T., Li, J., Chen, C., & Luo, D. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.822023 · Cited by 10 · see citing works
Jang, Y., Kang, S., Han, H. H., Kang, C. M., Cho, N. H., & Kim, B. G. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202402391 · Cited by 9 · see citing works
Self-citationFan, Y., Chiu, A., Zhao, F., & George, J. T. (2024) · Oncotarget · doi:10.18632/oncotarget.28666 · Cited by 9 · see citing works
Pattabiram, S., Gangadaran, P., Dhayalan, S., Chatterjee, G., Reyaz, D., Prakash, K., Arun, R., Rajendran, R. L., Ahn, B., & ArulJothi, K. N. (2025) · Current Issues in Molecular Biology · doi:10.3390/cimb47090730 · Cited by 8 · see citing works
Gommes, C., Louis, T., Bourgot, I., Noël, A., Blacher, S., & Maquoi, E. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.988502 · Cited by 8 · see citing works
Identifying the Pattern Characteristics of Anoikis-Related Genes in Keloid
Xie, R., Li, C., Yun, J., Zhang, S., Zhong, A., Cen, Y., Li, Z., & Chen, J. (2024) · Advances in Wound Care · doi:10.1089/wound.2024.0027 · Cited by 7 · see citing works
Heydari, F., Zendehdel, H., Varkiani, M. M., Fahmi, S., Derakhshani, M., Anvari, S., Farhid, F., Hamblin, M. R., & Naghinezhad, J. (2026) · Biomarker Research · doi:10.1186/s40364-026-00957-5 · Cited by 7 · see citing works
Gong, S. C., Cho, M., Lee, S. W., Kim, S. H., Kim, M. Y., & Baik, S. K. (2015) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.13063 · Cited by 6 · see citing works
Liu, Z., Tian, Y., Chen, Q., Zhang, G., Li, C., & Luo, D. (2019) · Anti-Cancer Agents in Medicinal Chemistry · doi:10.2174/1871520619666191212150322 · Cited by 6 · see citing works
Cavaco, A. C. M., & Eble, J. A. (2019) · Journal of Visualized Experiments · doi:10.3791/60122 · Cited by 5 · see citing works
Nodal metastasis signatures in breast cancer
Park, K., Lee, J. H., Han, H. H., Mun, S. G., Kang, S., Cha, Y. J., Koo, J. S., Kim, M. J., Lee, H. S., Moon, J., et al. (2016) · Pathology - Research and Practice · doi:10.1016/j.prp.2016.11.017 · Cited by 5 · see citing works
Self-citationLing, Z., Niego, B., Li, Q., Bhattaram, D., Villa, V. S., Hu, M. Y., Gong, Z., Smith, L. M., Frey, B. L., & Ren, X. (2025) · Advanced Materials · doi:10.1002/adma.202505445 · Cited by 4 · see citing works
Basement membrane-associated gene expression as a predictor of survival in oral cancer
Wang, X., Liu, C., Wu, H., Gu, Y., Zhang, L., Xu, R., & Lin, Q. (2024) · BMC Cancer · doi:10.1186/s12885-024-12485-2 · Cited by 4 · see citing works
Dysregulated gene subnetworks in breast invasive carcinoma reveal novel tumor suppressor genes
Agarwal, S., Parija, M., Naik, S. K., Kumari, P., Mishra, S. K., Adhya, A. K., Kashaw, S. K., & Dixit, A. (2024) · Scientific Reports · doi:10.1038/s41598-024-59953-0 · Cited by 4 · see citing works
Comprehensive pan-cancer analysis of LAMA3: implications for prognosis and immunotherapy
Huang, H. (2025) · American Journal of Translational Research · doi:10.62347/qyjw2277 · Cited by 4 · see citing works
Cadherin Expression and Progression of Squamous Cell Carcinomas of the Oral Cavity
Imai, K., Maeda, G., & Chib, T. (2012) · InTech eBooks · doi:10.5772/25407 · Cited by 4 · see citing works
Canlı, S. D. (2022) · Acta Medica · doi:10.32552/2022.actamedica.682 · Cited by 3 · see citing works
Sigston, E. A. W., Longano, A., Strzelecki, A. T., & Williams, B. R. G. (2016) · Head & Neck · doi:10.1002/hed.24450 · Cited by 3 · see citing works
Song, D., Kim, E., & Lee, S. E. (2020) · Archives of Pharmacal Research · doi:10.1007/s12272-020-01291-6 · Cited by 3 · see citing works
Song, H., Xu, J., Velázquez-Arcelay, K., Demirci, A., Raizenne, B. L., Hsu, S. C., Choi, J., Pham, J. H., Chen, Y.-A., Weinstein, H. N. W., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.25.711335 · Cited by 3 · see citing works
Immunpathogenese des Schleimhautpemphigoids
Schmidt, E., & Patzelt, S. (2023) · Die Ophthalmologie · doi:10.1007/s00347-023-01858-w · Cited by 2 · see citing works
Kim, J., Yu, J.-M., Bae, Y.-C., & Jung, J.-S. (2011) · Journal of Life Science · doi:10.5352/jls.2011.21.5.631 · Cited by 2 · see citing works
Abdel-Azeez, H. A., El-Hady, H., & Fikry, A. A. (2022) · Gastroenterology and hepatology from bed to bench. · Cited by 1 · see citing works
In vitro coculture models to study heterotypic interactions in breast cancer microenvironments
Casbas-Hernández, P. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/j1t4-4269 · Cited by 1 · see citing works
Agarwal, S., Naik, S., Kumari, P., Mishra, S. K., Adhya, A. K., Kashaw, S. K., & Dixit, A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.30.125260 · Cited by 1 · see citing works
The role of angiopoietin-like 4 in inflammation
Phua, T. (2017) · doi:10.32657/10356/72319
Laminin-511: a key regulator of breast cancer metastasis
Star, S. (2018) · Minerva Access (University of Melbourne)
Graudenz, M. S., Uchoa Diego, M., Cadore, E., Giacomazzi, J., & Maria, C.-J. S. (2019) · International Journal of Cancer and Clinical Research · doi:10.23937/2378-3419/1410103
Terabayashi, T., Hanada, K., Matsuoka, S., Sasaki, T., Katoh, A., Akamine, T., & Ishizaki, T. (2021) · Research Square · doi:10.21203/rs.3.rs-276535/v1
MicroRNA involvement in invasion and metastasis
Solé, C., Bielowski, A., & Lawrie, C. H. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-822287-4.00005-0
A New Frontier in Fighting Brain Cancer: Cutting Edge Magnetic Resonance Imaging Techniques
Nguyen, P., & Cain, J. A. (2022) · Journal of Student Research · doi:10.47611/jsrhs.v10i4.1952
Investigating the Prognosis Gene Profile of Triple-Negative Breast Cancer
Chang, Y.-T., Kao, L., Liao, G., Chen, Y., Hu, J., & Chang, Y.-T. (2022) · Journal of Medical Sciences · doi:10.4103/jmedsci.jmedsci_160_22
Modeling of the Tumor Microenvironment in Tumor Organoids
Shelkey, E., Dominijanni, A. J., Forsythe, S. D., Oommen, D., & Söker, S. (2022) · Royal Society of Chemistry eBooks · doi:10.1039/9781839166013-00279
Role of Laminin in Oral Carcinogenesis
Ahankare, P., Sridharan, G., & Patankar, S. R. (2019) · The Journal of Dentists · doi:10.12974/2311-8695.2019.07.4
Banerjee, M., Mishra, S., Vinukumar, G., Pandhari, M., Parimala, D. M., Sarvothama, M., Korlimarla, A., Srinath, B. S., & Bhat, R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.10.669320
Ozkan, M., White, M. J. V., Solanki, A., Pilling, D., Gomer, R. H., & Hubbell, J. A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.10.675333
Tümör-Bağışıklık Hücre Etkileşimlerini Araştırmak İçin Biyomühendisliksel Yöntemler
Topal, T., & Uzun, Z. E. (2025) · Gazi Üniversitesi Fen Fakültesi Dergisi · doi:10.63716/guffd.1768168
Stromal Laminin Subunit Alpha 3 is a Novel Prognostic Marker for Breast Cancer
Tan, Z., Liu, S., Zhao, D., Du, S., Sheng, C., Wang, H., & Lu, Z. (2026) · Clinical Medicine Insights Oncology · doi:10.1177/11795549261476199
Laminin – myCAF interplay promotes α6-integrin-mediated breast cancer cell invasion
Virumbrales-Muñoz, M., Fertal, S. A., Lugo-Cintrón, K. M., Loken, J. R., Vazquez, Y. N., Burkel, B. M., Zhang, J., Franck, C., Ayuso, J. M., Beebe, D. J., et al. (2026) · Lab on a Chip · doi:10.1039/d5lc00711a
- Authors
- Kim, B. G., An, H. J., Kang, S., Choi, Y. P., Gao, M.-Q., Park, H., & Cho, N. H.
- Affiliations
- Yonsei University (KR)
- CHA University (KR)
- Corresponding author
- Cho, Nam Hoon
- Venue
- The American Journal of Pathology
- Publisher
- Elsevier BV
- Published
- 2011-01
- Volume
- 178
- Issue
- 1
- Pages
- 373-381
- ISSN
- 0002-9440 (ISSN-L)
- PMC
- PMC3069863
- OpenAlex
- W2158186154
- Cited by
- 98
- References
- 37
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 6 · 2023: 9 · 2022: 8 · 2021: 4 · 2020: 5 · 2019: 14 · 2018: 6 · 2017: 3 · 2016: 5 · 2015: 5 · 2014: 3 · 2013: 8 · 2012: 5
- FWCI
- 3.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- American Journal Of Pathology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- YUHSpace (Yonsei University Medical Library) (submittedVersion, cc-by-nc-nd)
- Funders
- Ministry of Education, Science and Technology (2010-0000357)
- Ministry of Health and Welfare (A084550)
- National Research Foundation of Korea
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Health Sciences › Medicine › Pathology and Forensic Medicine › Breast Lesions and Carcinomas
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Keywords
- laminin-5, tumor microenvironment, tumor invasion, invasive ductal carcinoma, breast cancer, interface region, desmoplasia, epithelial-mesenchymal transition, myofibroblasts, extracellular matrix, matrix metalloproteinase-3, MT1-MMP, snails, ZEB1, N-cadherin, miR-200c, cancer-associated fibroblasts
- MeSH terms
- Snail Family Transcription Factors, Zinc Finger E-box-Binding Homeobox 1, Kalinin, Breast Neoplasms, Epithelial Cells, Female, Humans, Neoplasm Invasiveness, Transcription Factors, Cell Adhesion Molecules, Cadherins, Gene Expression Regulation, Neoplastic, Homeodomain Proteins, MicroRNAs, Integrin alpha6beta4, Matrix Metalloproteinase 14, Myofibroblasts, Epithelial-Mesenchymal Transition, Tumor Microenvironment
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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