دورية أكاديمية

E-cadherin staining in the diagnosis of lobular versus ductal neoplasms of the breast: the emperor has no clothes.

التفاصيل البيبلوغرافية
العنوان: E-cadherin staining in the diagnosis of lobular versus ductal neoplasms of the breast: the emperor has no clothes.
المؤلفون: Taha SR; Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA., Boulos F; Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA.
المصدر: Histopathology [Histopathology] 2024 Aug 13. Date of Electronic Publication: 2024 Aug 13.
Publication Model: Ahead of Print
نوع المنشور: Journal Article; Review
اللغة: English
بيانات الدورية: Publisher: Blackwell Scientific Publications Country of Publication: England NLM ID: 7704136 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-2559 (Electronic) Linking ISSN: 03090167 NLM ISO Abbreviation: Histopathology Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Oxford, Blackwell Scientific Publications.
مستخلص: Categorizing breast neoplasia as ductal or lobular is a daily exercise that relies on a combination of histologic and immunohistochemical tools. The historically robust link between loss of the E-cadherin molecule and lobular neoplasia has rendered staining for E-cadherin by immunohistochemistry a staple of this diagnostic process. Unfortunately, discordances between E-cadherin expression and histomorphology, and variations in E-cadherin staining patterns and intensities abound in clinical practice, but are often neglected in favour of a binary interpretation of the E-cadherin result. In this article, we highlight the complexities of E-cadherin expression through a review of the E-cadherin protein and its associated gene (CDH1), the mechanisms leading to aberrant/absent E-cadherin expression, and the implications of these factors on the reliability of the E-cadherin immunohistochemical stain in the classification of ductal versus lobular mammary neoplasia.
(© 2024 The Author(s). Histopathology published by John Wiley & Sons Ltd.)
References: Sledge GW, Chagpar A, Perou C. Collective wisdom: lobular carcinoma of the breast. Am. Soc. Clin. Oncol. Educ. Book 2016; 35; 18–21.
Cosar R, Sut N, Topaloglu S et al. Classifying invasive lobular carcinoma as special type breast cancer may be reducing its treatment success: a comparison of survival among invasive lobular carcinoma, invasive ductal carcinoma, and no‐lobular special type breast cancer. PLoS One 2023; 18; e0283445.
Rothschild HT, Clelland EN, Abel MK et al. The impact of histologic subtype on primary site surgery in the management of metastatic lobular versus ductal breast cancer: a population based study from the National Cancer Database (NCDB). Breast Cancer Res. Treat. 2024; 203(2); 245–256.
Oesterreich S, Nasrazadani A, Zou J et al. Clinicopathological features and outcomes comparing patients with invasive ductal and lobular breast cancer. J. Natl. Cancer Inst. 2022; 114; 1511–1522.
Kuba MG, Brogi E. Update on lobular lesions of the breast. Histopathology 2023; 82; 36–52.
Foote FW, Stewart FW. Lobular carcinoma in situ: a rare form of mammary cancer. Am. J. Pathol. 1941; 17; 491–496.3.
Moll R, Mitze M, Frixen UH, Birchmeier W. Differential loss of E‐cadherin expression in infiltrating ductal and lobular breast carcinomas. Am. J. Pathol. 1993; 143; 1731–1742.
Gamallo C, Palacios J, Suarez A et al. Correlation of E‐cadherin expression with differentiation grade and histological type in breast carcinoma. Am. J. Pathol. 1993; 142; 987–993.
Berx G, Cleton‐Jansen AM, Nollet F et al. E‐cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J. 1995; 14; 6107–6115.
Christgen M, Cserni G, Floris G et al. Lobular breast cancer: histomorphology and different concepts of a special Spectrum of tumors. Cancers (Basel) 2021; 13; 3695.
Canas‐Marques R, Schnitt SJ. E‐cadherin immunohistochemistry in breast pathology: uses and pitfalls. Histopathology 2016; 68; 57–69.
Sokolova A, Lakhani SR. Lobular carcinoma in situ: diagnostic criteria and molecular correlates. Mod. Pathol. 2021; 34(Suppl 1); 8–14.
McCart Reed AE, Kutasovic JR, Lakhani SR, Simpson PT. Invasive lobular carcinoma of the breast: morphology, biomarkers and 'omics. Breast Cancer Res. 2015; 17; 12.
Mahler‐Araujo B, Savage K, Parry S, Reis‐Filho JS. Reduction of E‐cadherin expression is associated with nonlobular breast carcinomas of basal‐like and triple negative phenotype. J. Clin. Pathol. 2008; 61; 615–620.
Da Silva L, Parry S, Reid L et al. Aberrant expression of E‐cadherin in lobular carcinomas of the breast. Am. J. Surg. Pathol. 2008; 32; 773–783.
Rakha EA, Patel A, Powe DG et al. Clinical and biological significance of E‐cadherin protein expression in invasive lobular carcinoma of the breast. Am. J. Surg. Pathol. 2010; 34; 1472–1479.
Acs G, Lawton TJ, Rebbeck TR, LiVolsi VA, Zhang PJ. Differential expression of E‐cadherin in lobular and ductal neoplasms of the breast and its biologic and diagnostic implications. Am. J. Clin. Pathol. 2001; 115; 85–98.
Choi YJ, Pinto MM, Hao L, Riba AK. Interobserver variability and aberrant E‐cadherin immunostaining of lobular neoplasia and infiltrating lobular carcinoma. Mod. Pathol. 2008; 21; 1224–1237.
Cserni G, Kálmán E, Udvarhelyi N et al. Evaluation of the routine use of E‐cadherin immunohistochemistry in the typing of breast carcinomas: results of a randomized diagnostic study. Histopathology 2023; 83; 810–821.
Christgen M, Kandt LD, Antonopoulos W et al. Inter‐observer agreement for the histological diagnosis of invasive lobular breast carcinoma. J. Pathol. Clin. Res. 2022; 8; 191–205.
van Roy F, Berx G. The cell‐cell adhesion molecule E‐cadherin. Cell. Mol. Life Sci. 2008; 65; 3756–3788.
Daulagala AC, Bridges MC, Kourtidis A. E‐cadherin beyond structure: a signaling hub in colon homeostasis and disease. Int. J. Mol. Sci. 2019; 20(11); 2756.
Tiwari P, Mrigwani A, Kaur H, Kaila P, Kumar R, Guptasarma P. Structural‐mechanical and biochemical functions of classical Cadherins at cellular junctions: a review and some hypotheses. Adv. Exp. Med. Biol. 2018; 1112; 107–138.
Pećina‐Slaus N. Tumor suppressor gene E‐cadherin and its role in normal and malignant cells. Cancer Cell Int. 2003; 3; 17.
Batra H, Mouabbi JA, Ding Q, Sahin AA, Raso MG. Lobular carcinoma of the breast: a comprehensive review with translational insights. Cancers (Basel) 2023; 15; 5491.
Schackmann RC, van Amersfoort M, Haarhuis JH et al. Cytosolic p120‐catenin regulates growth of metastatic lobular carcinoma through Rock1‐mediated anoikis resistance. J. Clin. Invest. 2011; 121; 3176–3188.
Dai Y, Zhang X, Ou Y et al. Anoikis resistance‐‐protagonists of breast cancer cells survive and metastasize after ECM detachment. Cell Commun. Signal 2023; 21; 190.
Corso G, Figueiredo J, De Angelis SP et al. E‐cadherin deregulation in breast cancer. J. Cell. Mol. Med. 2020; 24; 5930–5936.
Berx G, Cleton‐Jansen AM, Strumane K et al. E‐cadherin is inactivated in a majority of invasive human lobular breast cancers by truncation mutations throughout its extracellular domain. Oncogene 1996; 13; 1919–1925.
Ciriello G, Gatza ML, Beck AH et al. Comprehensive molecular portraits of invasive lobular breast cancer. Cell 2015; 163; 506–519.
Keller G, Vogelsang H, Becker I et al. Diffuse type gastric and lobular breast carcinoma in a familial gastric cancer patient with an E‐cadherin germline mutation. Am. J. Pathol. 1999; 155; 337–342.
Grabenstetter A, Mohanty AS, Rana S et al. E‐cadherin immunohistochemical expression in invasive lobular carcinoma of the breast: correlation with morphology and CDH1 somatic alterations. Hum. Pathol. 2020; 102; 44–53.
Ehrlich M. DNA hypermethylation in disease: mechanisms and clinical relevance. Epigenetics 2019; 14; 1141–1163.
Droufakou S, Deshmane V, Roylance R, Hanby A, Tomlinson I, Hart IR. Multiple ways of silencing E‐cadherin gene expression in lobular carcinoma of the breast. Int. J. Cancer 2001; 92; 404–408.
Sarrió D, Moreno‐Bueno G, Hardisson D et al. Epigenetic and genetic alterations of APC and CDH1 genes in lobular breast cancer: relationships with abnormal E‐cadherin and catenin expression and microsatellite instability. Int. J. Cancer 2003; 106; 208–215.
Lombaerts M, Middeldorp JW, van der Weide E et al. Infiltrating leukocytes confound the detection of E‐cadherin promoter methylation in tumors. Biochem. Biophys. Res. Commun. 2004; 319; 697–704.
Shinozaki M, Hoon DS, Giuliano AE et al. Distinct hypermethylation profile of primary breast cancer is associated with sentinel lymph node metastasis. Clin. Cancer Res. 2005; 11; 2156–2162.
Zou D, Yoon HS, Perez D, Weeks RJ, Guilford P, Humar B. Epigenetic silencing in nonneoplastic epithelia identifies E‐cadherin (CDH1) as a target for chemoprevention of lobular neoplasia. J. Pathol. 2009; 218; 265–272.
Liu J, Sun X, Qin S et al. CDH1 promoter methylation correlates with decreased gene expression and poor prognosis in patients with breast cancer. Oncol. Lett. 2016; 11; 2635–2643.
Alexander J, Mariani O, Meaudre C et al. Assessment of the molecular heterogeneity of E‐cadherin expression in invasive lobular breast cancer. Cancers (Basel) 2022; 14; 295.
Bücker L, Lehmann U. CDH1 (E‐cadherin) gene methylation in human breast cancer: critical appraisal of a long and twisted story. Cancers (Basel) 2022; 14; 4377.
Dopeso H, Gazzo AM, Derakhshan F et al. Genomic and epigenomic basis of breast invasive lobular carcinomas lacking CDH1 genetic alterations. NPJ Precis. Oncol. 2024; 8; 33.
Yu J, da Silva EM, La HS et al. Clinicopathologic and genomic features of lobular like invasive mammary carcinoma: is it a distinct entity? NPJ Breast Cancer 2023; 9; 60.
Prasad CP, Mirza S, Sharma G et al. Epigenetic alterations of CDH1 and APC genes: relationship with activation of Wnt/beta‐catenin pathway in invasive ductal carcinoma of breast. Life Sci. 2008; 83; 318–325.
Shargh SA, Sakizli M, Khalaj V et al. Downregulation of E‐cadherin expression in breast cancer by promoter hypermethylation and its relation with progression and prognosis of tumor. Med. Oncol. 2014; 31; 250.
Hoque MO, Prencipe M, Poeta ML et al. Changes in CpG islands promoter methylation patterns during ductal breast carcinoma progression. Cancer Epidemiol. Biomarkers Prev. 2009; 18; 2694–2700.
Felipe Lima J, Nofech‐Mozes S, Bayani J, Bartlett JM. EMT in breast carcinoma‐a review. J. Clin. Med. 2016; 5; 65.
Pastushenko I, Blanpain C. EMT transition states during tumor progression and metastasis. Trends Cell Biol. 2019; 29; 212–226.
Wu HT, Zhong HT, Li GW et al. Oncogenic functions of the EMT‐related transcription factor ZEB1 in breast cancer. J. Transl. Med. 2020; 18; 51.
Matysiak M, Kapka‐Skrzypczak L, Jodłowska‐Jędrych B, Kruszewski M. EMT promoting transcription factors as prognostic markers in human breast cancer. Arch. Gynecol. Obstet. 2017; 295; 817–825.
Qiao W, Jia Z, Liu H et al. Prognostic and clinicopathological value of twist expression in breast cancer: a meta‐analysis. PLoS One 2017; 12; e0186191.
de Herreros AG, Peiró S, Nassour M, Savagner P. Snail family regulation and epithelial mesenchymal transitions in breast cancer progression. J. Mammary Gland Biol. Neoplasia 2010; 15; 135–147.
Gould Rothberg BE, Bracken MB. E‐cadherin immunohistochemical expression as a prognostic factor in infiltrating ductal carcinoma of the breast: a systematic review and meta‐analysis. Breast Cancer Res. Treat. 2006; 100; 139–148.
Li Z, Yin S, Zhang L, Liu W, Chen B. Prognostic value of reduced E‐cadherin expression in breast cancer: a meta‐analysis. Oncotarget 2017; 8; 16445–16455.
Liu JB, Feng CY, Deng M et al. E‐cadherin expression phenotypes associated with molecular subtypes in invasive nonlobular breast cancer: evidence from a retrospective study and meta‐analysis. World J. Surg. Oncol. 2017; 15; 139.
McCart Reed AE, Kutasovic JR, Vargas AC et al. An epithelial to mesenchymal transition programme does not usually drive the phenotype of invasive lobular carcinomas. J. Pathol. 2016; 238; 489–494.
Derksen PW, Liu X, Saridin F et al. Somatic inactivation of E‐cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 2006; 10; 437–449.
Zhou F, Su J, Fu L et al. Unglycosylation at Asn‐633 made extracellular domain of E‐cadherin folded incorrectly and arrested in endoplasmic reticulum, then sequentially degraded by ERAD. Glycoconj. J. 2008; 25; 727–740.
Liwosz A, Lei T, Kukuruzinska MA. N‐glycosylation affects the molecular organization and stability of E‐cadherin junctions. J. Biol. Chem. 2006; 281; 23138–23149.
Pinho SS, Reis CA, Paredes J et al. The role of N‐acetylglucosaminyltransferase III and V in the post‐transcriptional modifications of E‐cadherin. Hum. Mol. Genet. 2009; 18; 2599–2608.
Pinho SS, Seruca R, Gärtner F et al. Modulation of E‐cadherin function and dysfunction by N‐glycosylation. Cell. Mol. Life Sci. 2011; 68; 1011–1020.
Zhu W, Leber B, Andrews DW. Cytoplasmic O‐glycosylation prevents cell surface transport of E‐cadherin during apoptosis. EMBO J. 2001; 20; 5999–6007.
Gu Y, Mi W, Ge Y et al. GlcNAcylation plays an essential role in breast cancer metastasis. Cancer Res. 2010; 70; 6344–6351.
Zhao H, Liang Y, Xu Z et al. N‐glycosylation affects the adhesive function of E‐cadherin through modifying the composition of adherens junctions (AJs) in human breast carcinoma cell line MDA‐MB‐435. J. Cell. Biochem. 2008; 104; 162–175.
Zhang H, Meng F, Wu S et al. Engagement of I‐branching {beta}‐1, 6‐N‐acetylglucosaminyltransferase 2 in breast cancer metastasis and TGF‐{beta} signaling. Cancer Res. 2011; 71; 4846–4856.
Wen R, Lin H, Li X, Lai X, Yang F. The regulatory mechanism of EpCAM N‐glycosylation‐mediated MAPK and PI3K/Akt pathways on epithelial‐mesenchymal transition in breast cancer cells. Cell. Mol. Biol. (Noisy‐le‐Grand) 2022; 68; 192–201.
David JM, Rajasekaran AK. Dishonorable discharge: the oncogenic roles of cleaved E‐cadherin fragments. Cancer Res. 2012; 72; 2917–2923.
Fujii T, Duarte S, Lee E, Ke B, Busuttil RW, Coito AJ. Tissue inhibitor of metalloproteinase 3 deficiency disrupts the hepatocyte E‐cadherin/β‐catenin complex and induces cell death in liver ischemia/reperfusion injury. Liver Transpl. 2020; 26; 113–126.
Mayerle J, Schnekenburger J, Krüger B et al. Extracellular cleavage of E‐cadherin by leukocyte elastase during acute experimental pancreatitis in rats. Gastroenterology 2005; 129; 1251–1267.
Devaux CA, Mezouar S, Mege JL. The E‐cadherin cleavage associated to pathogenic bacteria infections can favor bacterial invasion and transmigration, dysregulation of the immune response and cancer induction in humans. Front. Microbiol. 2019; 10; 2598.
Yasui H, Kawata T, Muramatsu K et al. Expression of N‐terminal‐deficient E‐cadherin protein in invasive lobular carcinoma of the breast. Am. J. Surg. Pathol. 2022; 46; 383–391.
Lei H, Sjöberg‐Margolin S, Salahshor S et al. CDH1 mutations are present in both ductal and lobular breast cancer, but promoter allelic variants show no detectable breast cancer risk. Int. J. Cancer 2002; 98; 199–204.
Zhang Z, Fang T, Lv Y. Prognostic and clinicopathological value of Slug protein expression in breast cancer: a systematic review and meta‐analysis. World J. Surg. Oncol. 2022; 20; 361.
Borst MJ, Ingold JA. Metastatic patterns of invasive lobular versus invasive ductal carcinoma of the breast. Surgery 1993; 114; 637–641. discussion 41‐2.
Thomas M, Kelly ED, Abraham J, Kruse M. Invasive lobular breast cancer: a review of pathogenesis, diagnosis, management, and future directions of early stage disease. Semin. Oncol. 2019; 46; 121–132.
Page DL, Jensen RA. Evaluation and management of high risk and premalignant lesions of the breast. World J. Surg. 1994; 18; 32–38.
Abdel‐Fatah TM, Powe DG, Hodi Z, Lee AH, Reis‐Filho JS, Ellis IO. High frequency of coexistence of columnar cell lesions, lobular neoplasia, and low grade ductal carcinoma in situ with invasive tubular carcinoma and invasive lobular carcinoma. Am. J. Surg. Pathol. 2007; 31; 417–426.
Simpson PT, Gale T, Reis‐Filho JS et al. Columnar cell lesions of the breast: the missing link in breast cancer progression? A morphological and molecular analysis. Am. J. Surg. Pathol. 2005; 29; 734–746.
Martinez V, Azzopardi JG. Invasive lobular carcinoma of the breast: incidence and variants. Histopathology 1979; 3; 467–488.
Rakha EA, Ellis IO. Lobular breast carcinoma and its variants. Semin. Diagn. Pathol. 2010; 27; 49–61.
Tan DS, Potts HW, Leong AC et al. The biological and prognostic significance of cell polarity and E‐cadherin in grade I infiltrating ductal carcinoma of the breast. J. Pathol. 1999; 189; 20–27.
Sivadas A, Kok VC, Ng KL. Multi‐omics analyses provide novel biological insights to distinguish lobular ductal types of invasive breast cancers. Breast Cancer Res. Treat. 2022; 193; 361–379.
Sun H, Ding Q, Sahin AA. Immunohistochemistry in the diagnosis and classification of breast tumors. Arch. Pathol. Lab Med. 2023; 147; 1119–1132.
Dabbs DJ, Schnitt SJ, Geyer FC et al. Lobular neoplasia of the breast revisited with emphasis on the role of E‐cadherin immunohistochemistry. Am. J. Surg. Pathol. 2013; 37; e1–e11.
Grote I, Bartels S, Christgen H et al. ERBB2 mutation is associated with sustained tumor cell proliferation after short‐term preoperative endocrine therapy in early lobular breast cancer. Mod. Pathol. 2022; 35; 1804–1811.
Derakhshan F, Da Cruz Paula A, Selenica P et al. Nonlobular invasive breast carcinomas with biallelic pathogenic CDH1 somatic alterations: a histologic, immunophenotypic, and genomic characterization. Mod. Pathol. 2023; 37; 100375.
Christgen M, Bartels S, van Luttikhuizen JL et al. E‐cadherin to P‐cadherin switching in lobular breast cancer with tubular elements. Mod. Pathol. 2020; 33; 2483–2498.
Palacios J, Benito N, Pizarro A et al. Anomalous expression of P‐cadherin in breast carcinoma. Correlation with E‐cadherin expression and pathological features. Am. J. Pathol. 1995; 146; 605–612.
Ribeiro AS, Sousa B, Carreto L et al. P‐cadherin functional role is dependent on E‐cadherin cellular context: a proof of concept using the breast cancer model. J. Pathol. 2013; 229; 705–718.
de Groot JS, Ratze MA, van Amersfoort M et al. αE‐catenin is a candidate tumor suppressor for the development of E‐cadherin‐expressing lobular‐type breast cancer. J. Pathol. 2018; 245; 456–467.
Brogi E. The morphologic spectrum of lobular carcinoma in situ (LCIS) observations on clinical significance, management implications and diagnostic pitfalls of classic, florid and pleomorphic LCIS. Virchows Arch. 2022; 481; 823–837.
WHO Classification of Tumours Editorial Board. WHO classification of tumours: breast tumours. Lyon: International Agency for Research on Cancer, 2019.
فهرسة مساهمة: Keywords: CDH1; E‐cadherin; IDC; ILC; breast cancer
تواريخ الأحداث: Date Created: 20240814 Latest Revision: 20240814
رمز التحديث: 20240814
DOI: 10.1111/his.15295
PMID: 39138705
قاعدة البيانات: MEDLINE
الوصف
تدمد:1365-2559
DOI:10.1111/his.15295