Claudin 1 in Breast Cancer: New Insights
Abstract
:1. Breast Cancer
1.1. Breast Cancer Progression and Metastasis
1.2. Epithelial Mesenchymal Transition (EMT)
2. Tight Junction (TJ) Proteins: The Claudins
3. Claudin 1
3.1. Dysregulation of Claudin 1 in Cancer
3.2. A Putative Tumor Suppressor Role in Invasive Human Breast Cancer
3.3. A Promoter of EMT, Cell Migration and Invasion
3.4. Interaction with the Extracellular Matrix
4. New Insights into the Role of Claudin 1 in Breast Cancer
4.1. A Leading Role in Collective Migration
4.2. More Than a Tumor Suppressor? “Claudin High” Breast Cancers
4.3. Cytoplasmic Mislocalization in Breast Cancer
4.4. Interaction with Unique Subcellular Partners
Protein | Description | Location | References |
---|---|---|---|
Ephrin B1 | A transmembrane protein involved in intrinsic cell signaling | Membrane | [113,114] |
ESCRT | Required for proper protein transport and maintenance of epithelial cell polarity | Cytoplasm | [115] |
CD9 | A transmembrane protein that plays a role in cell fusion and invasion | Membrane | [116] |
EpCAM | A transmembrane surface glycoprotein | Membrane | [117] |
5. Future Perspectives
Acknowledgments
Conflicts of Interest
References
- Canadian Cancer Society, Canadian Cancer Statistics 2014. Available online: http://www.cancer.ca (accessed on 15 November 2014).
- Curtis, C.; Shah, S.P.; Chin, S.F.; Turashvili, G.; Rueda, O.M.; Dunning, M.J.; Speed, D.; Lynch, A.G.; Samarajiwa, S.; Yuan, Y.; et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012, 486, 346–352. [Google Scholar] [CrossRef] [PubMed]
- Schnitt, S.J. Classification and prognosis of invasive breast cancer: From morphology to molecular taxonomy. Mod. Pathol. 2010, 23, S60–S64. [Google Scholar] [CrossRef] [PubMed]
- Perou, C.M.; Sorlie, T.; Eisen, M.B.; van de, R.M.; Jeffrey, S.S.; Rees, C.A.; Pollack, J.R.; Ross, D.T.; Johnsen, H.; Akslen, L.A.; et al. Molecular portraits of human breast tumours. Nature 2000, 406, 747–752. [Google Scholar] [CrossRef] [PubMed]
- Sorlie, T.; Perou, C.M.; Tibshirani, R.; Aas, T.; Geisler, S.; Johnsen, H.; Hastie, T.; Eisen, M.B.; van de Rijn, M.; Jeffrey, S.S.; et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. USA 2001, 98, 10869–10874. [Google Scholar] [CrossRef] [PubMed]
- Prat, A.; Parker, J.S.; Karginova, O.; Fan, C.; Livasy, C.; Herschkowitz, J.I.; He, X.; Perou, C.M. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res. 2010, 12. [Google Scholar] [CrossRef] [PubMed]
- Herschkowitz, J.I.; Simin, K.; Weigman, V.J.; Mikaelian, I.; Usary, J.; Hu, Z.; Rasmussen, K.E.; Jones, L.P.; Assefnia, S.; Chandrasekharan, S.; et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol. 2007, 8. [Google Scholar] [CrossRef] [PubMed]
- Lehmann, B.D.; Bauer, J.A.; Chen, X.; Sanders, M.E.; Chakravarthy, A.B.; Shyr, Y.; Pietenpol, J.A. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J. Clin. Investig. 2011, 121, 2750–2767. [Google Scholar] [CrossRef] [PubMed]
- Rodriguez-Pinilla, S.M.; Sarrio, D.; Honrado, E.; Hardisson, D.; Calero, F.; Benitez, J.; Palacios, J. Prognostic significance of basal-like phenotype and fascin expression in node-negative invasive breast carcinomas. Clin. Cancer Res. 2006, 12, 1533–1539. [Google Scholar] [CrossRef] [PubMed]
- Heimann, R.; Lan, F.; McBride, R.; Hellman, S. Separating favorable from unfavorable prognostic markers in breast cancer: The role of E-cadherin. Cancer Res. 2000, 60, 298–304. [Google Scholar] [PubMed]
- Weigelt, B.; Peterse, J.L.; vanʼt Veer, L.J. Breast cancer metastasis: Markers and models. Nat. Rev. Cancer 2005, 5, 591–602. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.C.; Sosnoski, D.M.; Mastro, A.M. Breast cancer metastasis to the bone: Mechanisms of bone loss. Breast Cancer Res. 2010, 12. [Google Scholar] [CrossRef] [PubMed]
- Mehlen, P.; Puisieux, A. Metastasis: A question of life or death. Nat. Rev. Cancer 2006, 6, 449–458. [Google Scholar] [CrossRef] [PubMed]
- Chambers, A.F.; Groom, A.C.; MacDonald, I.C. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2002, 2, 563–572. [Google Scholar] [CrossRef] [PubMed]
- Gupta, G.P.; Massagué, J. Cancer metastasis: Building a framework. Cell 2006, 127, 679–695. [Google Scholar] [CrossRef] [PubMed]
- Fidler, I.J. The pathogenesis of cancer metastasis: The “seed and soil” hypothesis revisited. Nat. Rev. Cancer 2003, 3, 453–458. [Google Scholar] [CrossRef] [PubMed]
- Fidler, I.J.; Talmadge, J.E. Evidence that intravenously derived murine pulmonary melanoma metastases can originate from the expansion of a single tumor cell. Cancer Res. 1986, 46, 5167–5171. [Google Scholar] [PubMed]
- Thiery, J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2002, 2, 442–454. [Google Scholar] [CrossRef] [PubMed]
- Guarino, M. Epithelial-mesenchymal transition and tumour invasion. Int. J. Biochem. Cell Biol. 2007, 39, 2153–2160. [Google Scholar] [CrossRef] [PubMed]
- Guarino, M.; Rubino, B.; Ballabio, G. The role of epithelial-mesenchymal transition in cancer pathology. Pathology 2007, 39, 305–318. [Google Scholar] [CrossRef] [PubMed]
- Kokkinos, M.I.; Wafai, R.; Wong, M.K.; Newgreen, D.F.; Thompson, E.W.; Waltham, M. Vimentin and epithelial-mesenchymal transition in human breast cancer—Observations in vitro and in vivo. Cells Tissues Organs 2007, 185, 191–203. [Google Scholar] [CrossRef] [PubMed]
- Lopez, D.; Niu, G.; Huber, P.; Carter, W.B. Tumor-induced upregulation of twist, snail, and slug represses the activity of the human ve-cadherin promoter. Arch. Biochem. Biophys. 2009, 482, 77–82. [Google Scholar] [CrossRef] [PubMed]
- Martinez-Estrada, O.M.; Culleres, A.; Soriano, F.X.; Peinado, H.; Bolos, V.; Martinez, F.O.; Reina, M.; Cano, A.; Fabre, M.; Vilaro, S. The transcription factors slug and snail act as repressors of claudin-1 expression in epithelial cells. Biochem. J. 2006, 394, 449–457. [Google Scholar] [CrossRef] [PubMed]
- Mironchik, Y.; Winnard, P.T.; Vesuna, F.; Kato, Y.; Wildes, F.; Pathak, A.P.; Kominsky, S.; Artemov, D.; Bhujwalla, Z.; Van Diest, P.; et al. Twist overexpression induces in vivo angiogenesis and correlates with chromosomal instability in breast cancer. Cancer Res. 2005, 65, 10801–10809. [Google Scholar] [CrossRef] [PubMed]
- Moody, S.E.; Perez, D.; Pan, T.-C.; Sarkisian, C.J.; Portocarrero, C.P.; Sterner, C.J.; Notorfrancesco, K.L.; Cardiff, R.D.; Chodosh, L.A. The transcriptional repressor snail promotes mammary tumor recurrence. Cancer Cell 2005, 8, 197–209. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Mani, S.A.; Donaher, J.L.; Ramaswamy, S.; Itzykson, R.A.; Come, C.; Savagner, P.; Gitelman, I.; Richardson, A.; Weinberg, R.A. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117, 927–939. [Google Scholar] [CrossRef] [PubMed]
- Blanchard, A.A.; Ma, X.; Dueck, K.J.; Penner, C.; Cooper, S.C.; Mulhall, D.; Murphy, L.C.; Leygue, E.; Myal, Y. Claudin 1 expression in basal-like breast cancer is related to patient age. BMC Cancer 2013, 13, 268. [Google Scholar] [CrossRef] [PubMed]
- Kwon, M.J. Emerging roles of claudins in human cancer. Int. J. Mol. Sci. 2013, 14, 18148–18180. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, X.; Zou, Y.; Gu, Q.; Zhao, G.; Gray, H.; Pfeffer, L.M.; Yue, J. Lentiviral vector mediated claudin1 silencing inhibits epithelial to mesenchymal transition in breast cancer cells. Viruses 2015, 7, 2965–2979. [Google Scholar] [CrossRef] [PubMed]
- Anderson, J.M.; Balda, M.S.; Fanning, A.S. The structure and regulation of tight junctions. Curr. Opin. Cell. Biol. 1993, 5, 772–778. [Google Scholar] [CrossRef]
- Hartsock, A.; Nelson, W.J. Adherens and tight junctions: Structure, function and connections to the actin cytoskeleton. Biochim. Biophys. Acta 2008, 1778, 660–669. [Google Scholar] [CrossRef] [PubMed]
- Suh, Y.; Yoon, C.H.; Kim, R.K.; Lim, E.J.; Oh, Y.S.; Hwang, S.G.; An, S.; Yoon, G.; Gye, M.C.; Yi, J.M.; et al. Claudin-1 induces epithelial-mesenchymal transition through activation of the c-Abl-ERK signaling pathway in human liver cells. Oncogene 2013, 32, 4873–4882. [Google Scholar] [CrossRef] [PubMed]
- Leech, A.O.; Cruz, R.G.; Hill, A.D.; Hopkins, A.M. Paradigms lost—An emerging role for over-expression of tight junction adhesion proteins in cancer pathogenesis. Ann. Transl. Med. 2015, 3. [Google Scholar] [CrossRef]
- Escudero-Esparza, A.; Jiang, W.G.; Martin, T.A. The claudin family and its role in cancer and metastasis. Front. Biosci. (Landmark. Ed.) 2011, 16, 1069–1083. [Google Scholar] [CrossRef] [PubMed]
- Gonzales-Mariscal, L. Tight Junctions, 2nd ed.; CRC Press: Boca Raton, FL, USA, 2001. [Google Scholar]
- Furuse, M.; Hata, M.; Furuse, K.; Yoshida, Y.; Haratake, A.; Sugitani, Y.; Noda, T.; Kubo, A.; Tsukita, S. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: A lesson from claudin-1-deficient mice. J. Cell. Biol. 2002, 156, 1099–1111. [Google Scholar] [CrossRef] [PubMed]
- Morin, P.J. Claudin proteins in human cancer: Promising new targets for diagnosis and therapy. Cancer Res. 2005, 65, 9603–9606. [Google Scholar] [CrossRef] [PubMed]
- Hewitt, K.J.; Agarwal, R.; Morin, P.J. The claudin gene family: Expression in normal and neoplastic tissues. BMC Cancer 2006, 6. [Google Scholar] [CrossRef] [PubMed]
- Morita, K.; Furuse, M.; Fujimoto, K.; Tsukita, S. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc. Natl. Acad. Sci. USA 1999, 96, 511–516. [Google Scholar] [CrossRef] [PubMed]
- Mrsny, R.J.; Brown, G.T.; Gerner-Smidt, K.; Buret, A.G.; Meddings, J.B.; Quan, C.; Koval, M.; Nusrat, A. A key claudin extracellular loop domain is critical for epithelial barrier integrity. Am. J. Pathol. 2008, 172, 905–915. [Google Scholar] [CrossRef] [PubMed]
- Colegio, O.R.; Van Itallie, C.; Rahner, C.; Anderson, J.M. Claudin extracellular domains determine paracellular charge selectivity and resistance but not tight junction fibril architecture. Am. J. Physiol. Cell. Physiol. 2003, 284, C1346–C1354. [Google Scholar] [CrossRef] [PubMed]
- Itoh, M.; Furuse, M.; Morita, K.; Kubota, K.; Saitou, M.; Tsukita, S. Direct binding of three tight junction-associated maguks, zo-1, zo-2, and zo-3, with the cooh termini of claudins. J. Cell. Biol. 1999, 147, 1351–1363. [Google Scholar] [CrossRef] [PubMed]
- Zahraoui, A.; Louvard, D.; Galli, T. Tight junction, a platform for trafficking and signaling protein complexes. J. Cell. Biol. 2000, 151, F31–F36. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, R.; Mori, Y.; Cheng, Y.; Jin, Z.; Olaru, A.V.; Hamilton, J.P.; David, S.; Selaru, F.M.; Yang, J.; Abraham, J.M.; et al. Silencing of claudin-11 is associated with increased invasiveness of gastric cancer cells. PLoS ONE 2009, 4, e8002. [Google Scholar] [CrossRef] [PubMed]
- Dhawan, P.; Singh, A.B.; Deane, N.G.; No, Y.; Shiou, S.-R.; Schmidt, C.; Neff, J.; Washington, M.K.; Beauchamp, R.D. Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer. J. Clin. Investig. 2005, 115, 1765–1776. [Google Scholar] [CrossRef] [PubMed]
- Kominsky, S.L.; Argani, P.; Korz, D.; Evron, E.; Raman, V.; Garrett, E.; Rein, A.; Sauter, G.; Kallioniemi, O.-P.; Sukumar, S. Loss of the tight junction protein claudin-7 correlates with histological grade in both ductal carcinoma in situ and invasive ductal carcinoma of the breast. Oncogene 2003, 22, 2021–2033. [Google Scholar] [CrossRef] [PubMed]
- Leotlela, P.D.; Wade, M.S.; Duray, P.H.; Rhode, M.J.; Brown, H.F.; Rosenthal, D.T.; Dissanayake, S.K.; Earley, R.; Indig, F.E.; Nickoloff, B.J.; et al. Claudin-1 overexpression in melanoma is regulated by pkc and contributes to melanoma cell motility. Oncogene 2007, 26, 3846–3856. [Google Scholar] [CrossRef] [PubMed]
- Michl, P.; Barth, C.; Buchholz, M.; Lerch, M.M.; Rolke, M.; Holzmann, K.H.; Menke, A.; Fensterer, H.; Giehl, K.; Lohr, M.; et al. Claudin-4 expression decreases invasiveness and metastatic potential of pancreatic cancer. Cancer Res. 2003, 63, 6265–6271. [Google Scholar] [PubMed]
- Singh, A.B.; Dhawan, P. Claudins and cancer: Fall of the soldiers entrusted to protect the gate and keep the barrier intact. Semin. Cell Dev. Biol. 2015, 42, 58–65. [Google Scholar] [CrossRef] [PubMed]
- Tsukita, S.; Furuse, M. Claudin-based barrier in simple and stratified cellular sheets. Curr. Opin. Cell. Biol. 2002, 14, 531–536. [Google Scholar] [CrossRef]
- Hamazaki, Y.; Itoh, M.; Sasaki, H.; Furuse, M.; Tsukita, S. Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. J. Biol. Chem. 2002, 277, 455–461. [Google Scholar] [CrossRef] [PubMed]
- Latorre, I.J.; Roh, M.H.; Frese, K.K.; Weiss, R.S.; Margolis, B.; Javier, R.T. Viral oncoprotein-induced mislocalization of select PDZ proteins disrupts tight junctions and causes polarity defects in epithelial cells. J. Cell Sci. 2005, 118, 4283–4293. [Google Scholar] [CrossRef] [PubMed]
- Nunbhakdi-Craig, V.; Craig, L.; Machleidt, T.; Sontag, E. Simian virus 40 small tumor antigen induces deregulation of the actin cytoskeleton and tight junctions in kidney epithelial cells. J. Virol. 2003, 77, 2807–2818. [Google Scholar] [CrossRef] [PubMed]
- Ohashi, M.; Sakurai, M.; Higuchi, M.; Mori, N.; Fukushi, M.; Oie, M.; Coffey, R.J.; Yoshiura, K.; Tanaka, Y.; Uchiyama, M.; et al. Human T-cell leukemia virus type 1 Tax oncoprotein induces and interacts with a multi-PDZ domain protein, MAGI-3. Virology 2004, 320, 52–62. [Google Scholar] [CrossRef] [PubMed]
- Evans, M.J.; von Hahn, T.; Tscherne, D.M.; Syder, A.J.; Panis, M.; Wölk, B.; Hatziioannou, T.; McKeating, J.A.; Bieniasz, P.D.; Rice, C.M. Claudin-1 is a hepatitis c virus co-receptor required for a late step in entry. Nature 2007, 446, 801–805. [Google Scholar] [CrossRef] [PubMed]
- Che, P.; Tang, H.; Li, Q. The interaction between claudin-1 and dengue viral prM/M protein for its entry. Virology 2013, 446, 303–313. [Google Scholar] [CrossRef] [PubMed]
- Offner, S.; Hekele, A.; Teichmann, U.; Weinberger, S.; Gross, S.; Kufer, P.; Itin, C.; Baeuerle, P.A.; Kohleisen, B. Epithelial tight junction proteins as potential antibody targets for pancarcinoma therapy. Cancer Immunol. Immunother. 2005, 54, 431–445. [Google Scholar] [CrossRef] [PubMed]
- Ayrolles-Torro, A.; Vezzio-Vie, N.; Denis, V.; Boissiere-Michot, F.; Garambois, V.; Busson, M.; Ait Arsa, I.; Mollevi, C.; Pugniere, M.; Bibeau, F.; et al. Abstract b245: Claudin-1 (CLDN1) as a new therapeutic target in colorectal cancer: Inhibition of cell growth and survival by an anti-CLDN1 monoclonal antibody. Mol. Cancer Ther. 2013, 12. [Google Scholar] [CrossRef]
- Fofana, I.; Krieger, S.E.; Grunert, F.; Glauben, S.; Xiao, F.; Fafi-Kremer, S.; Soulier, E.; Royer, C.; Thumann, C.; Mee, C.J.; et al. Monoclonal anti-claudin 1 antibodies prevent hepatitis C virus infection of primary human hepatocytes. Gastroenterology 2010, 139, 953–964. [Google Scholar] [CrossRef] [PubMed]
- Miyamoto, K.; Kusumi, T.; Sato, F.; Kawasaki, H.; Shibata, S.; Ohashi, M.; Hakamada, K.; Sasaki, M.; Kijima, H. Decreased expression of claudin-1 is correlated with recurrence status in esophageal squamous cell carcinoma. Biomed. Res. 2008, 29, 71–76. [Google Scholar] [CrossRef] [PubMed]
- Morohashi, S.; Kusumi, T.; Sato, F.; Odagiri, H.; Chiba, H.; Yoshihara, S.; Hakamada, K.; Sasaki, M.; Kijima, H. Decreased expression of claudin-1 correlates with recurrence status in breast cancer. Int. J. Mol. Med. 2007, 20, 139–143. [Google Scholar] [CrossRef] [PubMed]
- Chao, Y.C.; Pan, S.H.; Yang, S.C.; Yu, S.L.; Che, T.F.; Lin, C.W.; Tsai, M.S.; Chang, G.C.; Wu, C.H.; Wu, Y.Y.; et al. Claudin-1 is a metastasis suppressor and correlates with clinical outcome in lung adenocarcinoma. Am. J. Respir. Crit. Care Med. 2009, 179, 123–133. [Google Scholar] [CrossRef] [PubMed]
- Higashi, Y.; Suzuki, S.; Sakaguchi, T.; Nakamura, T.; Baba, S.; Reinecker, H.-C.; Nakamura, S.; Konno, H. Loss of claudin-1 expression correlates with malignancy of hepatocellular carcinoma. J. Surg. Res. 2007, 139, 68–76. [Google Scholar] [CrossRef] [PubMed]
- Kojima, T.; Takano, K.; Yamamoto, T.; Murata, M.; Son, S.; Imamura, M.; Yamaguchi, H.; Osanai, M.; Chiba, H.; Himi, T.; et al. Transforming growth factor-β induces epithelial to mesenchymal transition by down-regulation of claudin-1 expression and the fence function in adult rat hepatocytes. Liver Int. 2008, 28, 534–545. [Google Scholar] [CrossRef] [PubMed]
- Soini, Y.; Tommola, S.; Helin, H.; Martikainen, P. Claudins 1, 3, 4 and 5 in gastric carcinoma, loss of claudin expression associates with the diffuse subtype. Virchows Arch. 2006, 448, 52–58. [Google Scholar] [CrossRef] [PubMed]
- Pope, J.L.; Ahmad, R.; Bhat, A.A.; Washington, M.K.; Singh, A.B.; Dhawan, P. Claudin-1 overexpression in intestinal epithelial cells enhances susceptibility to adenamatous polyposis coli-mediated colon tumorigenesis. Mol. Cancer 2014, 13. [Google Scholar] [CrossRef] [PubMed]
- Takehara, M.; Nishimura, T.; Mima, S.; Hoshino, T.; Mizushima, T. Effect of claudin expression on paracellular permeability, migration and invasion of colonic cancer cells. Biol. Pharm. Bull. 2009, 32, 825–831. [Google Scholar] [CrossRef] [PubMed]
- De Oliveira, S.S.; de Oliveira, I.M.; de Souza, W.; Morgado-Diaz, J.A. Claudins upregulation in human colorectal cancer. FEBS Lett. 2005, 579, 6179–6185. [Google Scholar] [CrossRef] [PubMed]
- Kinugasa, T.; Huo, Q.U.N.; Higashi, D.; Shibaguchi, H.; Kuroki, M.; Tanaka, T.; Futami, K.; Yamashita, Y.; Hachimine, K.E.N.; Maekawa, S.; et al. Selective up-regulation of claudin-1 and claudin-2 in colorectal cancer. Anticancer Res. 2007, 27, 3729–3734. [Google Scholar] [CrossRef]
- Miwa, N.; Furuse, M.; Tsukita, S.; Niikawa, N.; Nakamura, Y.; Furukawa, Y. Involvement of claudin-1 in the β-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers. Oncol. Res. 2001, 12, 469–476. [Google Scholar] [CrossRef] [PubMed]
- Oku, N.; Sasabe, E.; Ueta, E.; Yamamoto, T.; Osaki, T. Tight junction protein claudin-1 enhances the invasive activity of oral squamous cell carcinoma cells by promoting cleavage of laminin-5 gamma2 chain via matrix metalloproteinase (MMP)-2 and membrane-type MMP-1. Cancer Res. 2006, 66, 5251–5257. [Google Scholar] [CrossRef] [PubMed]
- Sobel, G.; Nemeth, J.; Kiss, A.; Lotz, G.; Szabo, I.; Udvarhelyi, N.; Schaff, Z.; Paska, C. Claudin 1 differentiates endometrioid and serous papillary endometrial adenocarcinoma. Gynecol. Oncol. 2006, 103, 591–598. [Google Scholar] [CrossRef] [PubMed]
- Blanchard, A.A.; Skliris, G.P.; Watson, P.H.; Murphy, L.C.; Penner, C.; Tomes, L.; Young, T.L.; Leygue, E.; Myal, Y. Claudins 1, 3, and 4 protein expression in er negative breast cancer correlates with markers of the basal phenotype. Virchows Arch.: Int. J. Pathol. 2009, 454, 647–656. [Google Scholar] [CrossRef] [PubMed]
- Hoevel, T.; Macek, R.; Swisshelm, K.; Kubbies, M. Reexpression of the TJ protein CLDN1 induces apoptosis in breast tumor spheroids. Int. J. Cancer 2004, 108, 374–383. [Google Scholar] [CrossRef] [PubMed]
- Kulawiec, M.; Safina, A.; Desouki, M.M.; Still, I.; Matsui, S.I.; Bakin, A.; Singh, K.K. Tumorigenic transformation of human breast epithelial cells induced by mitochondrial DNA depletion. Cancer Biol. Ther. 2008, 7, 1732–1743. [Google Scholar] [CrossRef] [PubMed]
- Hoevel, T.; Macek, R.; Mundigl, O.; Swisshelm, K.; Kubbies, M. Expression and targeting of the tight junction protein CLDN1 in CLDN1-negative human breast tumor cells. J. Cell. Physiol. 2002, 191, 60–68. [Google Scholar] [CrossRef] [PubMed]
- Kramer, F.; White, K.; Kubbies, M.; Swisshelm, K.; Weber, B.H. Genomic organization of claudin-1 and its assessment in hereditary and sporadic breast cancer. Hum. Genet. 2000, 107, 249–256. [Google Scholar] [PubMed]
- Di Cello, F.; Cope, L.; Li, H.; Jeschke, J.; Wang, W.; Baylin, S.B.; Zahnow, C.A. Methylation of the claudin 1 promoter is associated with loss of expression in estrogen receptor positive breast cancer. PLoS ONE 2013, 8, e68630. [Google Scholar] [CrossRef] [PubMed]
- Myal, Y.B.A. Tight junctions in cancer: Multifaceted players in tumorigenesis and cancer progression. In Tight Junctions in Cancer Metastasis; Martin, T., Ed.; Springer: New York, NY, USA, 2012. [Google Scholar]
- Qin, W.; Ren, Q.; Liu, T.; Huang, Y.; Wang, J. Microrna-155 is a novel suppressor of ovarian cancer-initiating cells that targets CLDN1. FEBS Lett. 2013, 587, 1434–1439. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Mao, Q.; Liu, Y.; Hao, X.; Zhang, S.; Zhang, J. Analysis of miR-205 and miR-155 expression in the blood of breast cancer patients. Chin. J. Cancer Res. 2013, 25, 46–54. [Google Scholar] [PubMed]
- Roth, C.; Rack, B.; Muller, V.; Janni, W.; Pantel, K.; Schwarzenbach, H. Circulating micrornas as blood-based markers for patients with primary and metastatic breast cancer. Breast Cancer Res. 2010, 12. [Google Scholar] [CrossRef] [PubMed]
- Myal, Y.; Leygue, E.; Blanchard, A.A. Claudin 1 in breast tumorigenesis: Revelation of a possible novel “claudin high” subset of breast cancers. J. Biomed. Biotechnol. 2010, 2010. [Google Scholar] [CrossRef] [PubMed]
- Stebbing, J.; Filipovic, A.; Giamas, G. Claudin-1 as a promoter of emt in hepatocellular carcinoma. Oncogene 2013, 32, 4871–4872. [Google Scholar] [CrossRef] [PubMed]
- Singh, A.B.; Sharma, A.; Smith, J.J.; Krishnan, M.; Chen, X.; Eschrich, S.; Washington, M.K.; Yeatman, T.J.; Beauchamp, R.D.; Dhawan, P. Claudin-1 up-regulates the repressor ZEB-1 to inhibit E-cadherin expression in colon cancer cells. Gastroenterology 2011, 141, 2140–2153. [Google Scholar] [CrossRef] [PubMed]
- Lu, S.; Singh, K.; Mangray, S.; Tavares, R.; Noble, L.; Resnick, M.B.; Yakirevich, E. Claudin expression in high-grade invasive ductal carcinoma of the breast: Correlation with the molecular subtype. Mod. Pathol. 2013, 26, 485–495. [Google Scholar] [CrossRef] [PubMed]
- Hennessy, B.T.; Gonzalez-Angulo, A.-M.; Stemke-Hale, K.; Gilcrease, M.Z.; Krishnamurthy, S.; Lee, J.-S.; Fridlyand, J.; Sahin, A.; Agarwal, R.; Joy, C.; et al. Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res. 2009, 69, 4116–4124. [Google Scholar] [CrossRef] [PubMed]
- Sarrió, D.; Rodriguez-Pinilla, S.M.; Hardisson, D.; Cano, A.; Moreno-Bueno, G.; Palacios, J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res. 2008, 68, 989–997. [Google Scholar] [CrossRef] [PubMed]
- Zhou, B.; Blanchard, A.; Wang, N.; Ma, X.; Han, J.; Schroedter, I.; Leygue, E.; Myal, Y. Claudin 1 promotes migration and increases sensitivity to tamoxifen and anticancer drugs in luminal-like human breast cancer cells MCF7. Cancer Investig. 2015, 33, 429–439. [Google Scholar] [CrossRef] [PubMed]
- Batlle, E.; Sancho, E.; Franci, C.; Dominguez, D.; Monfar, M.; Baulida, J.; Garcia De, H.A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell. Biol. 2000, 2, 84–89. [Google Scholar] [CrossRef] [PubMed]
- Bolos, V. The transcription factor slug represses e-cadherin expression and induces epithelial to mesenchymal transitions: A comparison with snail and E47 repressors. J. Cell. Sci. 2002, 116, 499–511. [Google Scholar] [CrossRef]
- Shirakihara, T.; Saitoh, M.; Miyazono, K. Differential regulation of epithelial and mesenchymal markers by δEF1 proteins in epithelial mesenchymal transition induced by TGF-β. Mol. Biol. Cell 2007, 18, 3533–3544. [Google Scholar] [CrossRef] [PubMed]
- Comijn, J.; Berx, G.; Vermassen, P.; Verschueren, K.; van Grunsven, L.; Bruyneel, E.; Mareel, M.; Huylebroeck, D.; van Roy, F. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell. 2001, 7, 1267–1278. [Google Scholar] [CrossRef]
- Vesuna, F.; van Diest, P.; Chen, J.H.; Raman, V. Twist is a transcriptional repressor of E-cadherin gene expression in breast cancer. Biochem. Biophys. Res. Commun. 2008, 367, 235–241. [Google Scholar] [CrossRef] [PubMed]
- Hou, J.; Wang, Z.; Xu, H.; Yang, L.; Yu, X.; Yang, Z.; Deng, Y.; Meng, J.; Feng, Y.; Guo, X.; et al. Stanniocalicin 2 suppresses breast cancer cell migration and invasion via the PKC/claudin-1-mediated signaling. PLoS ONE 2015, 10, e0122179. [Google Scholar] [CrossRef] [PubMed]
- Aimes, R.T.; Quigley, J.P. Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4- and 1/4-length fragments. J. Biol. Chem. 1995, 270, 5872–5876. [Google Scholar] [PubMed]
- Ding, L.; Lu, Z.; Foreman, O.; Tatum, R.; Lu, Q.; Renegar, R.; Cao, J.; Chen, Y.H. Inflammation and disruption of the mucosal architecture in claudin-7-deficient mice. Gastroenterology 2012, 142, 305–315. [Google Scholar] [CrossRef] [PubMed]
- Miyamori, H.; Takino, T.; Kobayashi, Y.; Tokai, H.; Itoh, Y.; Seiki, M.; Sato, H. Claudin promotes activation of pro-matrix metalloproteinase-2 mediated by membrane-type matrix metalloproteinases. J. Biol. Chem. 2001, 276, 28204–28211. [Google Scholar] [CrossRef] [PubMed]
- Tsai, J.H.; Yang, J. Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes Dev. 2013, 27, 2192–2206. [Google Scholar] [CrossRef] [PubMed]
- Krakhmal, N.V.; Zavyalova, M.V.; Denisov, E.V.; Vtorushin, S.V.; Perelmuter, V.M. Cancer invasion: Patterns and mechanisms. Acta Nat. 2015, 7, 17–28. [Google Scholar]
- Friedl, P.; Gilmour, D. Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 2009, 10, 445–457. [Google Scholar] [CrossRef] [PubMed]
- Giampieri, S.; Manning, C.; Hooper, S.; Jones, L.; Hill, C.S.; Sahai, E. Localized and reversible TGFβ signalling switches breast cancer cells from cohesive to single cell motility. Nat. Cell. Biol. 2009, 11, 1287–1296. [Google Scholar] [CrossRef] [PubMed]
- Yilmaz, M.; Christofori, G. Mechanisms of motility in metastasizing cells. Mol. Cancer Res. 2010, 8, 629–642. [Google Scholar] [CrossRef] [PubMed]
- Friedl, P.; Noble, P.B.; Walton, P.A.; Laird, D.W.; Chauvin, P.J.; Tabah, R.J.; Black, M.; Zanker, K.S. Migration of coordinated cell clusters in mesenchymal and epithelial cancer explants in vitro. Cancer Res. 1995, 55, 4557–4560. [Google Scholar] [PubMed]
- Fortier, A.-M.; Asselin, E.; Cadrin, M. Keratin 8 and 18 loss in epithelial cancer cells increases collective cell migration and cisplatin sensitivity through claudin1 up-regulation. J. Biol. Chem. 2013, 288, 11555–11571. [Google Scholar] [CrossRef] [PubMed]
- Toft, D.J.; Cryns, V.L. Minireview: Basal-like breast cancer: From molecular profiles to targeted therapies. Mol. Endocrinol. 2011, 25, 199–211. [Google Scholar] [CrossRef] [PubMed]
- Heerma van Voss, M.R.; van Diest, P.J.; Smolders, Y.H.; Bart, J.; van der Wall, E.; van der Groep, P. Distinct claudin expression characterizes BRCA1-related breast cancer. Histopathology 2014, 65, 814–827. [Google Scholar] [CrossRef] [PubMed]
- Vincent-Salomon, A.; Gruel, N.; Lucchesi, C.; MacGrogan, G.; Dendale, R.; Sigal-Zafrani, B.; Longy, M.; Raynal, V.; Pierron, G.; de, M.I.; et al. Identification of typical medullary breast carcinoma as a genomic sub-group of basal-like carcinomas, a heterogeneous new molecular entity. Breast Cancer Res. 2007, 9. [Google Scholar] [CrossRef] [PubMed]
- Soini, Y. Expression of claudins 1, 2, 3, 4, 5 and 7 in various types of tumours. Histopathology 2005, 46, 551–560. [Google Scholar] [CrossRef] [PubMed]
- Tokés, A.-M.; Kulka, J.; Paku, S.; Szik, A.; Páska, C.; Novák, P.K.; Szilák, L.; Kiss, A.; Bögi, K.; Schaff, Z. Claudin-1, -3 and -4 proteins and mrna expression in benign and malignant breast lesions: A research study. Breast Cancer Res. 2005, 7. [Google Scholar] [CrossRef]
- Ruffer, C.; Gerke, V. The C-terminal cytoplasmic tail of claudins 1 and 5 but not its PDZ-binding motif is required for apical localization at epithelial and endothelial tight junctions. Eur. J. Cell. Biol. 2004, 83, 135–144. [Google Scholar] [CrossRef] [PubMed]
- French, A.D.; Fiori, J.L.; Camilli, T.C.; Leotlela, P.D.; OʼConnell, M.P.; Frank, B.P.; Subaran, S.; Indig, F.E.; Taub, D.D.; Weeraratna, A.T. PKC and PKA phosphorylation affect the subcellular localization of claudin-1 in melanoma cells. Int. J. Med. Sci. 2009, 6, 93–101. [Google Scholar] [CrossRef] [PubMed]
- Gonzales-Mariscal, L.; Garay, E.; Quiros, M. Regulation of claudins by posttranslational modifications and cell-signaling cascades. In Current Topics in Membranes; Elsevier Inc.: Burlington, MA, USA, 2010; Volume 65, pp. 113–150. [Google Scholar]
- Tanaka, M.; Kamata, R.; Sakai, R. Phosphorylation of ephrin-B1 via the interaction with claudin following cell-cell contact formation. EMBO J. 2005, 24, 3700–3711. [Google Scholar] [CrossRef] [PubMed]
- Dukes, J.D.; Fish, L.; Richardson, J.D.; Blaikley, E.; Burns, S.; Caunt, C.J.; Chalmers, A.D.; Whitley, P. Functional escrt machinery is required for constitutive recycling of claudin-1 and maintenance of polarity in vertebrate epithelial cells. Mol. Biol. Cell. 2011, 22, 3192–3205. [Google Scholar] [CrossRef] [PubMed]
- Kovalenko, O.V.; Yang, X.H.; Hemler, M.E. A novel cysteine cross-linking method reveals a direct association between claudin-1 and tetraspanin cd9. Mol. Cell. Proteom. 2007, 6, 1855–1867. [Google Scholar] [CrossRef] [PubMed]
- Wu, C.J.; Mannan, P.; Lu, M.; Udey, M.C. Epithelial cell adhesion molecule (EpCAM) regulates claudin dynamics and tight junctions. J. Biol. Chem. 2013, 288, 12253–12268. [Google Scholar] [CrossRef] [PubMed]
- Tanaka, M.; Sasaki, K.; Kamata, R.; Sakai, R. The C-terminus of ephrin-B1 regulates metalloproteinase secretion and invasion of cancer cells. J. Cell. Sci. 2007, 120, 2179–2189. [Google Scholar] [CrossRef] [PubMed]
- Xi, H.Q.; Wu, X.S.; Wei, B.; Chen, L. Eph receptors and ephrins as targets for cancer therapy. J. Cell. Mol. Med. 2012, 16, 2894–2909. [Google Scholar] [CrossRef] [PubMed]
- Schmidt, O.; Teis, D. The escrt machinery. Curr. Biol. 2012, 22, R116–R120. [Google Scholar] [CrossRef] [PubMed]
- Hanahan, D.; Weinberg, R.A. The hallmarks of cancer. Cell 2000, 100, 57–70. [Google Scholar] [CrossRef]
- Berditchevski, F.; Odintsova, E. Tetraspanins as regulators of protein trafficking. Traffic 2007, 8, 89–96. [Google Scholar] [CrossRef] [PubMed]
- Hemler, M.E. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu. Rev. Cell Dev. Biol. 2003, 19, 397–422. [Google Scholar] [CrossRef] [PubMed]
- Hemler, M.E. Tetraspanin functions and associated microdomains. Nat. Rev. Mol. Cell Biol. 2005, 6, 801–811. [Google Scholar] [CrossRef] [PubMed]
- Nydegger, S.; Khurana, S.; Krementsov, D.N.; Foti, M.; Thali, M. Mapping of tetraspanin-enriched microdomains that can function as gateways for HIV-1. J. Cell. Biol. 2006, 173, 795–807. [Google Scholar] [CrossRef] [PubMed]
- Boucheix, C.; Rubinstein, E. Tetraspanins. Cell. Mol. Life Sci. 2001, 58, 1189–1205. [Google Scholar] [CrossRef] [PubMed]
- Kischel, P.; Bellahcene, A.; Deux, B.; Lamour, V.; Dobson, R.; de Pauw, E.; Clezardin, P.; Castronovo, V. Overexpression of cd9 in human breast cancer cells promotes the development of bone metastases. Anticancer Res. 2012, 32, 5211–5220. [Google Scholar] [PubMed]
- Baeuerle, P.A.; Gires, O. Epcam (cd326) finding its role in cancer. Br. J. Cancer 2007, 96, 417–423. [Google Scholar] [CrossRef] [PubMed]
- Van der Gun, B.T.; Melchers, L.J.; Ruiters, M.H.; de Leij, L.F.; McLaughlin, P.M.; Rots, M.G. Epcam in carcinogenesis: The good, the bad or the ugly. Carcinogenesis 2010, 31, 1913–1921. [Google Scholar] [CrossRef] [PubMed]
- Freeman, M.E.; Kanyicska, B.; Lerant, A.; Nagy, G. Prolactin: Structure, function, and regulation of secretion. Physiol. Rev. 2000, 80, 1523–1631. [Google Scholar] [PubMed]
- Itoh, M.; Bissell, M.J. The organization of tight junctions in epithelia: Implications for mammary gland biology and breast tumorigenesis. J. Mammary Gland. Biol. Neoplasia 2003, 8, 449–462. [Google Scholar] [CrossRef] [PubMed]
- Martin, T.A.; Jiang, W.G. Loss of tight junction barrier function and its role in cancer metastasis. Biochim. Biophys. Acta 2009, 1788, 872–891. [Google Scholar] [CrossRef] [PubMed]
- Liu, S.; Yang, W.; Shen, L.; Turner, J.R.; Coyne, C.B.; Wang, T. Tight junction proteins claudin-1 and occludin control hepatitis c virus entry and are downregulated during infection to prevent superinfection. J. Virol. 2009, 83, 2011–2014. [Google Scholar] [CrossRef] [PubMed]
- Jahan, S.; Khaliq, S.; Samreen, B.; Ijaz, B.; Khan, M.; Ahmad, W.; Ashfaq, U.A.; Hassan, S. Effect of combined siRNA of HCV E2 gene and HCV receptors against HCV. Virol. J. 2011, 8, 295. [Google Scholar] [CrossRef] [PubMed]
- Charpin, C.; Tavassoli, F.; Secq, V.; Giusiano, S.; Villeret, J.; Garcia, S.; Birnbaum, D.; Bonnier, P.; Lavaut, M.N.; Boubli, L.; et al. Validation of an immunohistochemical signature predictive of 8-year outcome for patients with breast carcinoma. Int. J. Cancer 2012, 131, E236–E243. [Google Scholar] [CrossRef] [PubMed]
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Zhou, B.; Moodie, A.; Blanchard, A.A.A.; Leygue, E.; Myal, Y. Claudin 1 in Breast Cancer: New Insights. J. Clin. Med. 2015, 4, 1960-1976. https://doi.org/10.3390/jcm4121952
Zhou B, Moodie A, Blanchard AAA, Leygue E, Myal Y. Claudin 1 in Breast Cancer: New Insights. Journal of Clinical Medicine. 2015; 4(12):1960-1976. https://doi.org/10.3390/jcm4121952
Chicago/Turabian StyleZhou, Bowen, Amanda Moodie, Anne A. A. Blanchard, Etienne Leygue, and Yvonne Myal. 2015. "Claudin 1 in Breast Cancer: New Insights" Journal of Clinical Medicine 4, no. 12: 1960-1976. https://doi.org/10.3390/jcm4121952