Generic placeholder image

Clinical Cancer Drugs


ISSN (Print): 2212-697X
ISSN (Online): 2212-6988

Research Article

The Potential Role of Claudins in Regulation of Metastasis and Development of Drug Resistance in Breast Cancer

Author(s): Hemantkumar Patadia, Ankita Priyadarshini, Jay Ranade and Ajit Gangawane*

Volume 7, Issue 1, 2020

Page: [25 - 43] Pages: 19

DOI: 10.2174/2212697X06666191021121022


Background: Breast Cancer is a recurrent problem across the world. According to a report, breast cancer has the second highest mortality rate in women globally. Despite having an advanced degree of chemotherapy, resistance is developed against the therapies. Studies showed that anthracyclins like doxorubicin used in the treatment of breast cancer are found to develop resistance, which is not easy to identify. Mutations in the tumor suppressor gene P53 are associated with the primary resistance to doxorubicin and thus inducing an early relapse of breast tumors. Resistance against Doxorubicin is not identifiable easily. Development of resistance and metastasis of tumors are the two processes that cannot be separated from each other. It is widely known that endothelium has a major role in controlling metastasis and tumor cell invasion. Endothelial cells express different adhesion molecules during recruitment of leukocytes in localized area, which is called leukocyte extravasation or diapedesis, or leukocyte trans endothelial migration (LEM). LEM (leukocyte trans endothelial migration) plays crucial role in the inflammation of breast cancer tissues.

Objective: Predicting the role of deregulation of claudins in leukocyte trans endothelial migration in breast cancer metastasis and resistance.

Methods: The breast cancer proteomic metadata was collected and compared among the common candidates. The enrichment analysis of those common candidates was performed using a network analyst.

Results: The analysis of breast cancer genes obtained from dbDEPC showed probable involvement of 4 candidate genes belonging to the claudin family. Claudins are responsible for the migration of an increased amount of leukocytes in the breast tumor region, which increases the inflammation and may contribute to worsening the disease progression.

Conclusion: We believe these candidates also contribute in the development of resistance to chemotherapy.

Keywords: Leukocyte transendothelial migration, breast cancer, claudins, chemotherapy resistance, cancer resistance, metastasis.

Graphical Abstract
American Cancer Society. Cancer facts and figures 2017.
Aas T, Børresen AL, Geisler S, et al. Specific P53 mutations are associated with de novo resistance to doxorubicin in breast cancer patients. Nat Med 1996; 2(7): 811-4.
[] [PMID: 8673929]
Smith L, Watson MB, O’Kane SL, Drew PJ, Lind MJ, Cawkwell L. The analysis of doxorubicin resistance in human breast cancer cells using antibody microarrays. Mol Cancer Ther 2006; 5(8): 2115-20.
[] [PMID: 16928833]
Chang M. Tamoxifen resistance in breast cancer. Biomol Ther (Seoul) 2012; 20(3): 256-67.
[] [PMID: 24130921]
Tanic N, Milovanovic Z, Dzodic R, et al. The impact of PTEN tumor suppressor gene on acquiring resistance to tamoxifen treatment in breast cancer patients 2012. 4047
Ramos P, Bentires-Alj M. Mechanism-based cancer therapy: Resistance to therapy, therapy for resistance. Oncogene 2015; 34(28): 3617-26.
[] [PMID: 25263438]
Mierke CT. Role of the endothelium during tumor cell metastasis: Is the endothelium a barrier or a promoter for cell invasion and metastasis? J Biophys 2008.2008183516
[] [PMID: 20107573]
Gao A, Sun T, Ma G, et al. LEM4 confers tamoxifen resistance to breast cancer cells by activating cyclin D-CDK4/6-Rb and ERα pathway. Nat Commun 2018; 9(1): 4180.
[] [PMID: 30301939]
Leick M, Azcutia V, Newton G, Luscinskas FW. Leukocyte recruitment in inflammation: Basic concepts and new mechanistic insights based on new models and microscopic imaging technologies. Cell Tissue Res 2014; 355(3): 647-56.
[] [PMID: 24562377]
Strell C, Entschladen F. Extravasation of leukocytes in comparison to tumor cells. Cell Commun Signal 2008; 6: 10.
[] [PMID: 19055814]
Yang J, Rosen SD, Bendele P, Hemmerich S. Induction of PNAd and N-acetylglucosamine 6-O-sulfotransferases 1 and 2 in mouse collagen-induced arthritis. BMC Immunol 2006; 7: 12.
[] [PMID: 16772045]
Lasky LA, Singer MS, Dowbenko D, et al. An endothelial ligand for L-selectin is a novel mucin-like molecule. Cell 1992; 69(6): 927-38.
[] [PMID: 1376638]
Baumheter S, Singer M, Henzel W, et al. Binding of L-selectin to the vascular sialomucin CD34 Science 1993; 262(5132): 436-8.
Umemoto E, Tanaka T, Kanda H, et al. Nepmucin, a novel HEV sialomucin, mediates L-selectin-dependent lymphocyte rolling and promotes lymphocyte adhesion under flow. J Exp Med 2006; 203(6): 1603-14.
[] [PMID: 16754720]
Hemmerich S, Butcher EC, Rosen SD. Sulfation-dependent recognition of high endothelial venules (HEV)-ligands by L-selectin and MECA 79, and adhesion-blocking monoclonal antibody. J Exp Med 1994; 180(6): 2219-26.
[] [PMID: 7525849]
Hanley WD, Napier SL, Burdick MM, Schnaar RL, Sackstein R, Konstantopoulos K. Variant isoforms of CD44 are P- and L-selectin ligands on colon carcinoma cells. FASEB J 2006; 20(2): 337-9.
[] [PMID: 16352650]
Barthel SR, Gavino JD, Descheny L, Dimitroff CJ. Targeting selectins and selectin ligands in inflammation and cancer. Expert Opin Ther Targets 2007; 11(11): 1473-91.
[] [PMID: 18028011]
Schweitzer KM, Dräger AM, van der Valk P, et al. Constitutive expression of E-selectin and vascular cell adhesion molecule-1 on endothelial cells of hematopoietic tissues. Am J Pathol 1996; 148(1): 165-75.
[PMID: 8546203]
Dimitroff CJ, Descheny L, Trujillo N, et al. Identification of leukocyte E-selectin ligands, P-selectin glycoprotein ligand-1 and E-selectin ligand-1, on human metastatic prostate tumor cells. Cancer Res 2005; 65(13): 5750-60.
[] [PMID: 15994950]
Thomas SN, Zhu F, Schnaar RL, Alves CS, Konstantopoulos K. Carcinoembryonic antigen and CD44 variant isoforms cooperate to mediate colon carcinoma cell adhesion to E- and L-selectin in shear flow. J Biol Chem 2008; 283(23): 15647-55.
[] [PMID: 18375392]
Strell C, Lang K, Niggemann B, Zaenker KS, Entschladen F. Surface molecules regulating rolling and adhesion to endothelium of neutrophil granulocytes and MDA-MB-468 breast carcinoma cells and their interaction. Cell Mol Life Sci 2007; 64(24): 3306-16.
[] [PMID: 17994288]
Qi J, Chen N, Wang J, Siu CH. Transendothelial migration of melanoma cells involves N-cadherin-mediated adhesion and activation of the β-catenin signaling pathway. Mol Biol Cell 2005; 16(9): 4386-97.
[] [PMID: 15987741]
Borsig L, Wong R, Feramisco J, Nadeau DR, Varki NM, Varki A. Heparin and cancer revisited: Mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis. Proc Natl Acad Sci USA 2001; 98(6): 3352-7.
[] [PMID: 11248082]
Kim YJ, Borsig L, Han HL, Varki NM, Varki A. Distinct selectin ligands on colon carcinoma mucins can mediate pathological interactions among platelets, leukocytes, and endothelium. Am J Pathol 1999; 155(2): 461-72.
[] [PMID: 10433939]
Strilic B, Offermanns S. Intravascular survival and extravasation of tumor cells. Cancer Cell 2017; 32(3): 282-93.
[] [PMID: 28898694]
Schumacher D, Strilic B, Sivaraj KK, Wettschureck N, Offermanns S. Platelet-derived nucleotides promote tumor-cell transendothelial migration and metastasis via P2Y2 receptor. Cancer Cell 2013; 24(1): 130-7.
[] [PMID: 23810565]
Gassmann P, Haier J, Schlüter K, et al. CXCR4 regulates the early extravasation of metastatic tumor cells in vivo. Neoplasia 2009; 11(7): 651-61.
[] [PMID: 19568410]
Martin MD, Kremers GJ, Short KW, et al. Rapid extravasation and establishment of breast cancer micrometastases in the liver microenvironment. Mol Cancer Res 2010; 8(10): 1319-27.
[] [PMID: 20724460]
Kienast Y, von Baumgarten L, Fuhrmann M, et al. Real-time imaging reveals the single steps of brain metastasis formation. Nat Med 2010; 16(1): 116-22.
[] [PMID: 20023634]
Tremblay PL, Huot J, Auger FA. Mechanisms by which E-selectin regulates diapedesis of colon cancer cells under flow conditions. Cancer Res 2008; 68(13): 5167-76.
[] [PMID: 18593916]
Muller WA. Mechanisms of transendothelial migration of leukocytes. Circ Res 2009; 105(3): 223-30.
[] [PMID: 19644057]
Muller WA. Mechanisms of leukocyte transendothelial migration. Annu Rev Pathol 2011; 6: 323-44.
[] [PMID: 21073340]
Lukas Z, Dvorak K. Adhesion molecules in biology and oncology. Acta Vet Brno 2004; 73: 93-104.
Rosenstein Y, Park JK, Hahn WC, Rosen FS, Bierer BE, Burakoff SJ. CD43, a molecule defective in Wiskott-Aldrich syndrome, binds ICAM-1. Nature 1991; 354(6350): 233-5.
[] [PMID: 1683685]
Regimbald LH, Pilarski LM, Longenecker BM, Reddish MA, Zimmermann G, Hugh JC. The breast mucin MUCI as a novel adhesion ligand for endothelial intercellular adhesion molecule 1 in breast cancer. Cancer Res 1996; 56(18): 4244-9.
[PMID: 8797599]
Huang MT, Larbi KY, Hanschen M, Nourshargh S. ICAM-2 mediates PECAM-1-independent neutrophil transmigration in vivo. FASEB J 2005; 107(12): 4721-7.
[PMID: 16469869]
Woodfin A, Voisin MB, Imhof BA, Dejana E, Engelhardt B, Nourshargh S. Endothelial cell activation leads to neutrophil transmigration as supported by the sequential roles of ICAM-2, JAM-A, and PECAM-1. Blood 2009; 113(24): 6246-57.
[] [PMID: 19211506]
Hotárková S, Hermanová M, Povýsilová V, et al. Demonstration of MyoD1 expression in oncocytic cardiomyopathy: Report of two cases and review of the literature. Pathol Res Pract 2004; 200(1): 59-65.
[] [PMID: 15157052]
Muller WA, Weigl SA, Deng X, Phillips DM. PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med 1993; 178(2): 449-60.
[] [PMID: 8340753]
Mamdouh Z, Chen X, Pierini LM, Maxfield FR, Muller WA. Targeted recycling of PECAM from endothelial surface-connected compartments during diapedesis. Nature 2003; 421(6924): 748-53.
[] [PMID: 12610627]
Muller WA. PECAM: Regulating the start of diapedesis. In: Adhesion molecules: Function and inhibition. Basel: Birkhauser Verlag AG 2007; pp. 201-20.
Keiper T, Santoso S, Nawroth PP, Orlova V, Chavakis T. The role of junctional adhesion molecules in cell-cell interactions. Histol Histopathol 2005; 20(1): 197-203.
[PMID: 15578438]
Ostermann G, Weber KSC, Zernecke A, Schröder A, Weber C. JAM-1 is a ligand of the beta(2) integrin LFA-1 involved in transendothelial migration of leukocytes. Nat Immunol 2002; 3(2): 151-8.
[] [PMID: 11812992]
Johnson-Léger CA, Aurrand-Lions M, Beltraminelli N, Fasel N, Imhof BA. Junctional adhesion molecule-2 (JAM-2) promotes lymphocyte transendothelial migration. Blood 2002; 100(7): 2479-86.
[] [PMID: 12239159]
Chavakis T, Keiper T, Matz-Westphal R, et al. The junctional adhesion molecule-C promotes neutrophil transendothelial migration in vitro and in vivo. J Biol Chem 2004; 279(53): 55602-8.
[] [PMID: 15485832]
Liu Y, Nusrat A, Schnell FJ, et al. Human junction adhesion molecule regulates tight junction resealing in epithelia. J Cell Sci 2000; 113(Pt 13): 2363-74.
[PMID: 10852816]
Schenkel AR, Mamdouh Z, Muller WA. Locomotion of monocytes on endothelium is a critical step during extravasation. Nat Immunol 2004; 5(4): 393-400.
[] [PMID: 15021878]
Maître JL, Heisenberg CP. Three functions of cadherins in cell adhesion. Curr Biol 2013; 23(14): R626-33.
[] [PMID: 23885883]
Ivanov DB, Philippova MP, Tkachuk VA. Structure and functions of classical cadherins. Biochemistry (Mosc) 2001; 66(10): 1174-86.
[] [PMID: 11736639]
Luo B-H, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol 2007; 25: 619-47.
[] [PMID: 17201681]
Buckley CD, Rainger GE, Bradfield PF, Nash GB, Simmons DL. Cell adhesion: More than just glue. (review) Mol Membr Biol 1998; 15(4): 167-76.
[] [PMID: 10087503]
Khalili AA, Ahmad MR. A Review of cell adhesion studies for biomedical and biological applications. Int J Mol Sci 2015; 16(8): 18149-84.
[] [PMID: 26251901]
Senapati S, Das S, Batra SK. Mucin-interacting proteins: From function to therapeutics. Trends Biochem Sci 2010; 35(4): 236-45.
[] [PMID: 19913432]
Rivalland G, Loveland B, Mitchell P. Update on Mucin-1 immunotherapy in cancer: A clinical perspective. Expert Opin Biol Ther 2015; 15(12): 1773-87.
[] [PMID: 26453294]
Hayashi T, Takahashi T, Motoya S, et al. MUC1 mucin core protein binds to the domain 1 of ICAM-1. Digestion 2001; 63(Suppl. 1): 87-92.
[] [PMID: 11173916]
Rahn JJ, Chow JW, Horne GJ, et al. MUC1 mediates transendothelial migration in vitro by ligating endothelial cell ICAM-1. Clin Exp Metastasis 2005; 22(6): 475-83.
[] [PMID: 16320110]
Alkhamesi NA, Roberts G, Ziprin P, Peck DH, Darzi AW. Induction of proteases in peritoneal carcinomatosis, the Role of ICAM-1/CD43 Interaction. Biomark Insights 2007; 2: 377-84.
[] [PMID: 19662219]
Matsumoto M, Atarashi K, Umemoto E, et al. CD43 functions as a ligand for E-Selectin on activated T cells. J Immunol 2005; 175(12): 8042-50.
[] [PMID: 16339541]
Schenkel AR, Mamdouh Z, Chen X, Liebman RM, Muller WA. CD99 plays a major role in the migration of monocytes through endothelial junctions. Nat Immunol 2002; 3(2): 143-50.
[] [PMID: 11812991]
Lou O, Alcaide P, Luscinskas FW, Muller WA. CD99 is a key mediator of the transendothelial migration of neutrophils. J Immunol 2007; 178(2): 1136-43.
[] [PMID: 17202377]
Dasgupta B, Dufour E, Mamdouh Z, Muller WA. A novel and critical role for tyrosine 663 in platelet endothelial cell adhesion molecule-1 trafficking and transendothelial migration. J Immunol 2009; 182(8): 5041-51.
[] [PMID: 19342684]
Osanai M, Takasawa A, Murata M, Sawada N. Claudins in cancer: Bench to bedside. Pflugers Arch 2017; 469(1): 55-67.
[] [PMID: 27624415]
Krishnan M, Singh AB, Smith JJ, et al. HDAC inhibitors regulate claudin-1 expression in colon cancer cells through modulation of mRNA stability. Oncogene 2010; 29(2): 305-12.
[] [PMID: 19881542]
Wang H, Yang X. The expression patterns of tight junction protein claudin-1, -3, and -4 in human gastric neoplasms and adjacent non-neoplastic tissues. Int J Clin Exp Pathol 2015; 8(1): 881-7.
[PMID: 25755790]
Chao YC, Pan SH, Yang SC, et al. Claudin-1 is a metastasis suppressor and correlates with clinical outcome in lung adenocarcinoma. Am J Respir Crit Care Med 2009; 179(2): 123-33.
[] [PMID: 18787218]
Szász AM, Nyirády P, Majoros A, et al. beta-catenin expression and claudin expression pattern as prognostic factors of prostatic cancer progression. BJU Int 2010; 105(5): 716-22.
[] [PMID: 19818082]
Szasz AM, Tokes AM, Micsinai M, et al. Prognostic significance of claudin expression changes in breast cancer with regional lymph node metastasis. Clin Exp Metastasis 2011; 28(1): 55-63.
[] [PMID: 20963473]
Kim TH, Huh JH, Lee S, Kang H, Kim GI, An HJ. Down-regulation of claudin-2 in breast carcinomas is associated with advanced disease. Histopathology 2008; 53(1): 48-55.
[] [PMID: 18479414]
Kimbung S, Kovács A, Bendahl PO, et al. Claudin-2 is an independent negative prognostic factor in breast cancer and specifically predicts early liver recurrences. Mol Oncol 2014; 8(1): 119-28.
[] [PMID: 24287398]
Micke P, Mattsson JS, Edlund K, et al. Aberrantly activated claudin 6 and 18.2 as potential therapy targets in non-small-cell lung cancer. Int J Cancer 2014; 135(9): 2206-14.
[] [PMID: 24710653]
Sheehan GM, Kallakury BV, Sheehan CE, Fisher HA, Kaufman RP Jr, Ross JS. Loss of claudins-1 and -7 and expression of claudins-3 and -4 correlate with prognostic variables in prostatic adenocarcinomas. Hum Pathol 2007; 38(4): 564-9.
[] [PMID: 17306334]
Rangel LB, Agarwal R, D’Souza T, et al. Tight junction proteins claudin-3 and claudin-4 are frequently overexpressed in ovarian cancer but not in ovarian cystadenomas. Clin Cancer Res 2003; 9(7): 2567-75.
[PMID: 12855632]
Choi YL, Kim J, Kwon MJ, et al. Expression profile of tight junction protein claudin 3 and claudin 4 in ovarian serous adenocarcinoma with prognostic correlation. Histol Histopathol 2007; 22(11): 1185-95.
[PMID: 17647191]
Kleinberg L, Holth A, Trope CG, Reich R, Davidson B. Claudin upregulation in ovarian carcinoma effusions is associated with poor survival. Hum Pathol 2008; 39(5): 747-57.
[] [PMID: 18439941]
Tabariès S, Siegel PM. The role of claudins in cancer metastasis. Oncogene 2017; 36(9): 1176-90.
[] [PMID: 27524421]
Schimmel L, Heemskerk N, van Buul JD. Leukocyte transendothelial migration: A local affair. Small GTPases 2017; 8(1): 1-15.
[] [PMID: 27715453]
Proteomics database for breast cancer
Oliveros JC. (2007-2015) Venny.. An interactive tool for comparing lists with Venn’s diagrams Available at: http://bioinfogp.cnb.
Zhou G, Soufan O, Ewald J, Hancock REW, Basu N, Xia J. NetworkAnalyst 3.0: A visual analytics platform for comprehensive gene expression profiling and meta-analysis. Nucleic Acids Res 2019; 47(W1)W234-41
[] [PMID: 30931480]
Xia J, Gill EE, Hancock REW. NetworkAnalyst for statistical, visual and network-based meta-analysis of gene expression data. Nat Protoc 2015; 10(6): 823-44.
[] [PMID: 25950236]
Kanehisa M, Sato Y, Furumichi M, Morishima K, Tanabe M. New approach for understanding genome variations in KEGG. Nucleic Acids Res 2019; 47(D1): D590-5.
[] [PMID: 30321428]
Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes nucleic acids res 2000; 28(1): 27-30.
Angelow S, Ahlstrom R, Yu ASL. Biology of claudins. Am J Physiol Renal Physiol 2008; 295(4): F867-76.
[] [PMID: 18480174]
Furuse M, Fujimoto K, Sato N, Hirase T, Tsukita S, Tsukita S. Overexpression of occludin, a tight junction-associated integral membrane protein, induces the formation of intracellular multilamellar bodies bearing tight junction-like structures. J Cell Sci 1996; 109(Pt 2): 429-35.
[PMID: 8838666]
Simon DB, Lu Y, Choate KA, et al. Paracellin-1, a renal tight junction protein required for paracellular Mg2+ resorption. Science 1999; 285(5424): 103-6.
Krause G, Winkler L, Mueller SL, Haseloff RF, Piontek J, Blasig IE. Structure and function of claudins. Biochim Biophys Acta 2008; 1778(3): 631-45.
[] [PMID: 18036336]
Kitajiri SI, Furuse M, Morita K, et al. Expression patterns of claudins, tight junction adhesion molecules, in the inner ear. Hear Res 2004; 187(1-2): 25-34.
[] [PMID: 14698084]
Morin PJ. Claudin proteins in human cancer: Promising new targets for diagnosis and therapy. Cancer Res 2005; 65(21): 9603-6.
[] [PMID: 16266975]
Daugherty BL, Ward C, Smith T, Ritzenthaler JD, Koval M. Regulation of heterotypic claudin compatibility. J Biol Chem 2007; 282(41): 30005-13.
[] [PMID: 17699514]
Weinstein RS, Merk FB, Alroy J. The structure and function of intercellular junctions in cancer. Adv Cancer Res 1976; 23: 23-89.
[] [PMID: 179291]
Soler AP, Miller RD, Laughlin KV, Carp NZ, Klurfeld DM, Mullin JM. Increased tight junctional permeability is associated with the development of colon cancer. Carcinogenesis 1999; 20(8): 1425-31.
[] [PMID: 10426787]
Mullin JM. Potential interplay between luminal growth factors and increased tight junction permeability in epithelial carcinogenesis. J Exp Zool 1997; 279(5): 484-9.
[<484::AID-JEZ11>3.0.CO;2-8] [PMID: 9392870]
Martìn-Padura I, Lostaglio S, Schneemann M, et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 1998; 142(1): 117-27.
[] [PMID: 9660867]
D’Souza T, Agarwal R, Morin PJ. Phosphorylation of claudin-3 at threonine 192 by cAMP-dependent protein kinase regulates tight junction barrier function in ovarian cancer cells. J Biol Chem 2005; 280(28): 26233-40.
[] [PMID: 15905176]
Krämer F, White K, Kubbies M, Swisshelm K, Weber BHF. Genomic organization of claudin-1 and its assessment in hereditary and sporadic breast cancer. Hum Genet 2000; 107(3): 249-56.
[] [PMID: 11071387]
Tokés AM, Kulka J, Paku S, et al. Claudin-1, -3 and -4 proteins and mRNA expression in benign and malignant breast lesions: a research study. Breast Cancer Res 2005; 7(2): R296-305.
[] [PMID: 15743508]
Ma F, Ding X, Fan Y, et al. A CLDN1-negative phenotype predicts poor prognosis in triple-negative breast cancer. PLoS One 2014; 9(11): e112765
[] [PMID: 25393310]
Morohashi S, Kusumi T, Sato F, et al. Decreased expression of claudin-1 correlates with recurrence status in breast cancer. Int J Mol Med 2007; 20(2): 139-43.
[] [PMID: 17611630]
Blanchard AA, Skliris GP, Watson PH, et al. Claudins 1, 3, and 4 protein expression in ER negative breast cancer correlates with markers of the basal phenotype. Virchows Arch 2009; 454(6): 647-56.
[] [PMID: 19387682]
Kominsky SL, Vali M, Korz D, et al. Clostridium perfringens enterotoxin elicits rapid and specific cytolysis of breast carcinoma cells mediated through tight junction proteins claudin 3 and 4. Am J Pathol 2004; 164(5): 1627-33.
[] [PMID: 15111309]
Katahira J, Sugiyama H, Inoue N, Horiguchi Y, Matsuda M, Sugimoto N. Clostridium perfringens enterotoxin utilizes two structurally related membrane proteins as functional receptors in vivo. J Biol Chem 1997; 272(42): 26652-8.
[] [PMID: 9334247]
Lu S, Singh K, Mangray S, et al. Claudin expression in high-grade invasive ductal carcinoma of the breast: Correlation with the molecular subtype. Mod Pathol 2013; 26(4): 485-95.
[] [PMID: 23222490]
Kulka J, Szász AM, Németh Z, et al. Expression of tight junction protein claudin-4 in basal-like breast carcinomas. Pathol Oncol Res 2009; 15(1): 59-64.
[] [PMID: 18752049]
Herschkowitz JI, Simin K, Weigman VJ, et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 2007; 8(5): R76.
[] [PMID: 17493263]
Prat A, Parker JS, Karginova O, et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010; 12(5): R68.
[] [PMID: 20813035]
Lehmann BD, Bauer JA, Chen X, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011; 121(7): 2750-67.
[] [PMID: 21633166]
Wang F, Gao Y, Tang L, et al. A novel PAK4-CEBPB-CLDN4 axis involving in breast cancer cell migration and invasion. Biochem Biophys Res Commun 2019; 511(2): 404-8.
[] [PMID: 30808546]
Yoshida H, Sumi T, Zhi X, Yasui T, Honda K, Ishiko O. Claudin-4: A potential therapeutic target in chemotherapy-resistant ovarian cancer. Anticancer Res 2011; 31(4): 1271-7.
[PMID: 21508375]
Hennessy BT, Gonzalez-Angulo AM, Stemke-Hale K, et al. Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res 2009; 69(10): 4116-24.
[] [PMID: 19435916]
Creighton CJ, Li X, Landis M, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA 2009; 106(33): 13820-5.
[] [PMID: 19666588]
Hu A, Li J, Ruan S, Fan Y, Liao Y. Polymorphisms in CLDN1 are associated with age and differentiation of triple-negative breast cancer patients. Biosci Rep 2019; 39(4): BSR20181952
[] [PMID: 30910845]
Zhou S, Piao X, Wang C, Wang R, Song Z. Identification of claudin-1, -3, -7 and -8 as prognostic markers in human laryngeal carcinoma. Mol Med Rep 2019; 20(1): 393-400.
[] [PMID: 31115553]
Bella J, Kolatkar PR, Marlor CW, Greve JM, Rossmann MG. The structure of the two amino-terminal domains of human ICAM-1 suggests how it functions as a rhinovirus receptor and as an LFA-1 integrin ligand. Proc Natl Acad Sci USA 1998; 95(8): 4140-5.
[] [PMID: 9539703]
Huang MT, Larbi KY, Scheiermann C, et al. ICAM-2 mediates neutrophil transmigration in vivo: Evidence for stimulus specificity and a role in PECAM-1-independent transmigration. Blood 2006; 107(12): 4721-7.
[] [PMID: 16469869]
Itoh M, Sasaki H, Furuse M, Ozaki H, Kita T, Tsukita S. Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J Cell Biol 2001 Aug 6;; 154(3): 491-7.
Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA. Mucins in the mucosal barrier to infection. Mucosal Immunol 2008; 1(3): 183-97.
[] [PMID: 19079178]
Matter K, Aijaz S, Tsapara A, Balda MS. Mammalian tight junctions in the regulation of epithelial differentiation and proliferation. Curr Opin Cell Biol 2005; 17(5): 453-8.
Martin TA, Jiang WG. Tight junctions and their role in cancer metastasis. Histol Histopathol 2001; 16(4): 1183-95.
[PMID: 11642738]
Blanchard AA, Zelinski T, Xie J, et al. Identification of claudin 1 transcript variants in human invasive breast cancer. PLoS One 2016 Sep 20; ; 11(9): e0163387
Kwon MJ. Emerging roles of claudins in human cancer 2013; 18148-80.
Lanigan F, McKiernan E, Brennan DJ, et al. Increased claudin-4 expression is associated with poor prognosis and high tumour grade in breast cancer. Int J Cancer 2009; 124(9): 2088-97.
[] [PMID: 19142967]
Morrow M, Burstein HJ, Harris JR. Ch 79: Malignant tumors of the breast.10th ed.2015 DeVita, Hellman, and Rosenberg’s Cancer: Priciples and practice of ontology..
Al-Mehdi AB, Tozawa K, Fisher AB, Shientag L, Lee A, Muschel RJ. Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: A new model for metastasis. Nat Med 2000; 6(1): 100-2.
[] [PMID: 10613833]
Stoletov K, Kato H, Zardouzian E, et al. Visualizing extravasation dynamics of metastatic tumor cells. J Cell Sci 2010; 123(Pt 13): 2332-41.
[] [PMID: 20530574]

© 2022 Bentham Science Publishers | Privacy Policy