Invasive lobular carcinoma of the breast: Morphology, biomarkers and 'omics

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  Reed, McCart E ^a   Kutasovic, Jamie R ^a   Lakhani, Sunil R ^a,b,c   Simpson, Peter T ^a,c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b Pathology Queensland   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; UVOMORULIN; CADHERIN; TUMOR MARKER;

ALGORITHM; BREAST CARCINOMA; CANCER DIAGNOSIS; CANCER MORPHOLOGY; HUMAN; IMMUNOPHENOTYPING; MORPHOLOGICAL TRAIT; REVIEW; ANIMAL; BREAST NEOPLASMS; CARCINOMA, LOBULAR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; PHENOTYPE; PROGNOSIS; PROTEOMICS; TUMOR INVASION;

ALGORITHMS; ANIMALS; BIOMARKERS, TUMOR; BREAST NEOPLASMS; CADHERINS; CARCINOMA, LOBULAR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMICS; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; NEOPLASM INVASIVENESS; PHENOTYPE; PROGNOSIS; PROTEOMICS;

EID: 84924246744     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-015-0519-x     Document Type: Review

References (73)

1. Ferlicot S, Vincent-Salomon A, Medioni J, Genin P, Rosty C, Sigal-Zafrani B, et al. Wide metastatic spreading in infiltrating lobular carcinoma of the breast. Eur J Cancer. 2004;40:336-41.
2. Rakha EA, El-Sayed ME, Powe DG, Green AR, Habashy H, Grainge MJ, et al. Invasive lobular carcinoma of the breast: response to hormonal therapy and outcomes. Eur J Cancer. 2008;44:73-83.
3. Pestalozzi BC, Zahrieh D, Mallon E, Gusterson BA, Price KN, Gelber RD, et al. Distinct clinical and prognostic features of infiltrating lobular carcinoma of the breast: combined results of 15 International Breast Cancer Study Group clinical trials. J Clin Oncol. 2008;26:3006-14.
4. Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van de Vijver MJ. WHO Classification of Tumours of the Breast. 4th ed. Lyon: IARC; 2012.
5. Haagensen CD, Lane N, Lattes R, Bodian C. Lobular neoplasia (so-called lobular carcinoma in situ) of the breast. Cancer. 1978;42:737-69.
6. Page DL, Kidd Jr TE, Dupont WD, Simpson JF, Rogers LW. Lobular neoplasia of the breast: higher risk for subsequent invasive cancer predicted by more extensive disease. Hum Pathol. 1991;22:1232-9.
7. Sneige N, Wang J, Baker BA, Krishnamurthy S, Middleton LP. Clinical, histopathologic, and biologic features of pleomorphic lobular (ductal-lobular) carcinoma in situ of the breast: a report of 24 cases. Mod Pathol. 2002;15:1044-50.
8. Shin SJ, Lal A, De Vries S, Suzuki J, Roy R, Hwang ES, et al. Florid lobular carcinoma in situ: molecular profiling and comparison to classic lobular carcinoma in situ and pleomorphic lobular carcinoma in situ. Hum Pathol. 2013;44:1998-2009.
9. Rakha EA, Gill MS, El-Sayed ME, Khan MM, Hodi Z, Blamey RW, et al. The biological and clinical characteristics of breast carcinoma with mixed ductal and lobular morphology. Breast Cancer Res Treat. 2009;114:243-50.
10. Rakha EA, Ellis IO. Lobular breast carcinoma and its variants. Semin Diagn Pathol. 2010;27:49-61.
11. Iorfida M, Maiorano E, Orvieto E, Maisonneuve P, Bottiglieri L, Rotmensz N, et al. Invasive lobular breast cancer: subtypes and outcome. Breast Cancer Res Treat. 2012;133:713-23.
12. Rakha EA, van Deurzen CH, Paish EC, Macmillan RD, Ellis IO, Lee AH. Pleomorphic lobular carcinoma of the breast: is it a prognostically significant pathological subtype independent of histological grade? Mod Pathol. 2013;26:496-501.
13. 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;31:417-26.
14. Reis-Filho JS, Simpson PT, Jones C, Steele D, Mackay A, Iravani M, et al. Pleomorphic lobular carcinoma of the breast: role of comprehensive molecular pathology in characterization of an entity. J Pathol. 2005;207:1-13.
15. Vos CB, Cleton-Jansen AM, Berx G, de Leeuw WJ, ter Haar NT, van Roy F, et al. E-cadherin inactivation in lobular carcinoma in situ of the breast: an early event in tumorigenesis. Br J Cancer. 1997;76:1131-3.
16. Arpino G, Bardou VJ, Clark GM, Elledge RM. Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cancer Res. 2004;6:R149-56.
17. Sastre-Garau X, Jouve M, Asselain B, Vincent-Salomon A, Beuzeboc P, Dorval T, et al. Infiltrating lobular carcinoma of the breast. Clinicopathologic analysis of 975 cases with reference to data on conservative therapy and metastatic patterns. Cancer. 1996;77:113-20.
18. Simpson PT, Reis-Filho JS, Lambros MB, Jones C, Steele D, Mackay A, et al. Molecular profiling pleomorphic lobular carcinomas of the breast: evidence for a common molecular genetic pathway with classic lobular carcinomas. J Pathol. 2008;215:231-44.
19. Skliris GP, Munot K, Bell SM, Carder PJ, Lane S, Horgan K, et al. Reduced expression of oestrogen receptor beta in invasive breast cancer and its re-expression using DNA methyl transferase inhibitors in a cell line model. J Pathol. 2003;201:213-20.
20. Rakha EA, Patel A, Powe DG, Benhasouna A, Green AR, Lambros MB, et al. Clinical and biological significance of E-cadherin protein expression in invasive lobular carcinoma of the breast. Am J Surg Pathol. 2010;34:1472-9.
21. Berx G, Cleton-Jansen AM, Strumane K, de Leeuw WJ, Nollet F, van Roy F, et al. E-cadherin is inactivated in a majority of invasive human lobular breast cancers by truncation mutations throughout its extracellular domain. Oncogene. 1996;13:1919-25.
22. Da Silva L, Parry S, Reid L, Keith P, Waddell N, Kossai M, et al. Aberrant expression of E-cadherin in lobular carcinomas of the breast. Am J Surg Pathol. 2008;32:773-83.
23. Reis-Filho JS, Simpson PT, Turner NC, Lambros MB, Jones C, Mackay A, et al. FGFR1 emerges as a potential therapeutic target for lobular breast carcinomas. Clin Cancer Res. 2006;12:6652-62.
24. Dabbs DJ, Bhargava R, Chivukula M. Lobular versus ductal breast neoplasms: the diagnostic utility of p120 catenin. Am J Surg Pathol. 2007;31:427-37.
25. Schackmann RC, van Amersfoort M, Haarhuis JH, Vlug EJ, Halim VA, Roodhart JM, et al. Cytosolic p120-catenin regulates growth of metastatic lobular carcinoma through Rock1-mediated anoikis resistance. J Clin Invest. 2011;121:3176-88.
26. Dabbs DJ, Schnitt SJ, Geyer FC, Weigelt B, Baehner FL, Decker T, et al. Lobular neoplasia of the breast revisited with emphasis on the role of E-cadherin immunohistochemistry. Am J Surg Pathol. 2013;37:e1-11.
27. 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;92:404-8.
28. Sarrio D, Moreno-Bueno G, Hardisson D, Sanchez-Estevez C, Guo M, Herman JG, 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;106:208-15.
29. Zou D, Yoon HS, Perez D, Weeks RJ, Guilford P, Humar B. Epigenetic silencing in non-neoplastic epithelia identifies E-cadherin (CDH1) as a target for chemoprevention of lobular neoplasia. J Pathol. 2009;218:265-72.
30. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2:401-4.
31. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6:pl1.
32. Simpson PT, Reis-Filho JS, Gale T, Lakhani SR. Molecular evolution of breast cancer. J Pathol. 2005;205:248-54.
33. Lu YJ, Osin P, Lakhani SR, Di Palma S, Gusterson BA, Shipley JM. Comparative genomic hybridization analysis of lobular carcinoma in situ and atypical lobular hyperplasia and potential roles for gains and losses of genetic material in breast neoplasia. Cancer Res. 1998;58:4721-7.
34. Chen YY, Hwang ES, Roy R, DeVries S, Anderson J, Wa C, et al. Genetic and phenotypic characteristics of pleomorphic lobular carcinoma in situ of the breast. Am J Surg Pathol. 2009;33:1683-94.
35. Mastracci TL, Tjan S, Bane AL, O'Malley FP, Andrulis IL. E-cadherin alterations in atypical lobular hyperplasia and lobular carcinoma in situ of the breast. Mod Pathol. 2005;18:741-51.
36. Cleton-Jansen AM. E-cadherin and loss of heterozygosity at chromosome 16 in breast carcinogenesis: different genetic pathways in ductal and lobular breast cancer? Breast Cancer Res. 2002;4:5-8.
37. Network CGA. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490:61-70.
38. Ellis MJ, Ding L, Shen D, Luo J, Suman VJ, Wallis JW, et al. Whole-genome analysis informs breast cancer response to aromatase inhibition. Nature. 2012;486:353-60.
39. Guilford P, Hopkins J, Harraway J, McLeod M, McLeod N, Harawira P, et al. E-cadherin germline mutations in familial gastric cancer. Nature. 1998;392:402-5.
40. Schrader KA, Masciari S, Boyd N, Salamanca C, Senz J, Saunders DN, et al. Germline mutations in CDH1 are infrequent in women with early-onset or familial lobular breast cancers. J Med Genet. 2011;48:64-8.
41. Petridis C, Shinomiya I, Kohut K, Gorman P, Caneppele M, Shah V, et al. Germline CDH1 mutations in bilateral lobular carcinoma in situ. Br J Cancer. 2014;110:1053-7.
42. Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B, 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;10:437-49.
43. Humar B, Blair V, Charlton A, More H, Martin I, Guilford P. E-cadherin deficiency initiates gastric signet-ring cell carcinoma in mice and man. Cancer Res. 2009;69:2050-6.
44. Christgen M, Derksen PW. Lobular breast cancer: molecular basis, mouse and cellular models. Breast Cancer Res. in press.
45. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117:927-39.
46. Sarrio D, Rodriguez-Pinilla SM, Hardisson D, Cano A, Moreno-Bueno G, Palacios J. Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res. 2008;68:989-97.
47. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature. 2000;406:747-52.
48. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res. 2010;12:R68.
49. Mackay A, Weigelt B, Grigoriadis A, Kreike B, Natrajan R, A'Hern R, et al. Microarray-based class discovery for molecular classification of breast cancer: analysis of interobserver agreement. J Natl Cancer Inst. 2011;103:662-73.
50. Weigelt B, Horlings HM, Kreike B, Hayes MM, Hauptmann M, Wessels LF, et al. Refinement of breast cancer classification by molecular characterization of histological special types. J Pathol. 2008;216:141-50.
51. Gruel N, Lucchesi C, Raynal V, Rodrigues MJ, Pierron G, Goudefroye R, et al. Lobular invasive carcinoma of the breast is a molecular entity distinct from luminal invasive ductal carcinoma. Eur J Cancer. 2010;46:2399-407.
52. Korkola JE, DeVries S, Fridlyand J, Hwang ES, Estep AL, Chen YY, et al. Differentiation of lobular versus ductal breast carcinomas by expression microarray analysis. Cancer Res. 2003;63:7167-75.
53. Turashvili G, Bouchal J, Baumforth K, Wei W, Dziechciarkova M, Ehrmann J, et al. Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis. BMC Cancer. 2007;7:55.
54. Weigelt B, Geyer FC, Natrajan R, Lopez-Garcia MA, Ahmad AS, Savage K, et al. The molecular underpinning of lobular histological growth pattern: a genome-wide transcriptomic analysis of invasive lobular carcinomas and grade- and molecular subtype-matched invasive ductal carcinomas of no special type. J Pathol. 2010;220:45-57.
55. Zhao H, Langerod A, Ji Y, Nowels KW, Nesland JM, Tibshirani R, et al. Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Mol Biol Cell. 2004;15:2523-36.
56. McCart Reed AE, Song S, Kutasovic JR, Reid LE, Valle JM, Vargas AC, et al. Thrombospondin-4 expression is activated during the stromal response to invasive breast cancer. Virchows Arch. 2013;463:535-45.
57. Loo LW, Grove DI, Williams EM, Neal CL, Cousens LA, Schubert EL, et al. Array comparative genomic hybridization analysis of genomic alterations in breast cancer subtypes. Cancer Res. 2004;64:8541-9.
58. Roylance R, Gorman P, Papior T, Wan YL, Ives M, Watson JE, et al. A comprehensive study of chromosome 16q in invasive ductal and lobular breast carcinoma using array CGH. Oncogene. 2006;25:6544-53.
59. Sircoulomb F, Nicolas N, Ferrari A, Finetti P, Bekhouche I, Rousselet E, et al. ZNF703 gene amplification at 8p12 specifies luminal B breast cancer. EMBO Mol Med. 2011;3:153-66.
60. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature. 2012;486:346-52.
61. Shah SP, Morin RD, Khattra J, Prentice L, Pugh T, Burleigh A, et al. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature. 2009;461:809-13.
62. Ross JS, Wang K, Sheehan CE, Boguniewicz AB, Otto G, Downing SR, et al. Relapsed classic E-cadherin (CDH1)-mutated invasive lobular breast cancer shows a high frequency of HER2 (ERBB2) gene mutations. Clin Cancer Res. 2013;19:2668-76.
63. Hilleren DJ, Andersson IT, Lindholm K, Linnell FS. Invasive lobular carcinoma: mammographic findings in a 10-year experience. Radiology. 1991;178:149-54.
64. Niell B, Specht M, Gerade B, Rafferty E. Is excisional biopsy required after a breast core biopsy yields lobular neoplasia? AJR Am J Roentgenol. 2012;199:929-35.
65. Rakha EA, El-Sayed ME, Menon S, Green AR, Lee AH, Ellis IO. Histologic grading is an independent prognostic factor in invasive lobular carcinoma of the breast. Breast Cancer Res Treat. 2008;111:121-7.
66. Gluz O, Hofmann D, Wurstlein R, Liedtke C, Nitz U, Harbeck N. Genomic Profiling in Luminal Breast Cancer. Breast Care (Basel). 2013;8:414-22.
67. Jeselsohn R, Yelensky R, Buchwalter G, Frampton G, Meric-Bernstam F, Gonzalez-Angulo AM, et al. Emergence of constitutively active estrogen receptor-alpha mutations in pretreated advanced estrogen receptor-positive breast cancer. Clin Cancer Res. 2014;20:1757-67.
68. Sikora MJ, Cooper KL, Bahreini A, Luthra S, Wang G, Chandran UR, et al. Invasive lobular carcinoma cell lines are characterized by unique estrogen-mediated gene expression patterns and altered tamoxifen response. Cancer Res. 2014;74:1463-74.
69. Riggins RB, Lan JP, Zhu Y, Klimach U, Zwart A, Cavalli LR, et al. ERRgamma mediates tamoxifen resistance in novel models of invasive lobular breast cancer. Cancer Res. 2008;68:8908-17.
70. Christgen M, Noskowicz M, Schipper E, Christgen H, Heil C, Krech T, et al. Oncogenic PIK3CA mutations in lobular breast cancer progression. Genes Chromosomes Cancer. 2013;52:69-80.
71. Miller TW, Balko JM, Arteaga CL. Phosphatidylinositol 3-kinase and antiestrogen resistance in breast cancer. J Clin Oncol. 2011;29:4452-61.
72. Arthur LM, Turnbull AK, Webber VL, Larionov AA, Renshaw L, Kay C, et al. Molecular changes in lobular breast cancers in response to endocrine therapy. Cancer Res. 2014;74:5371-6.
73. Metzger O, Giobbie-Hurder A, Mallon E, Viale G, Winer E, Thürlimann B, et al. Relative effectiveness of letrozole compared with tamoxifen for patients with lobular carcinoma in the BIG 1-98 trial [abstract]. In: Thirty-Fifth Annual CTRC-AACR San Antonio Breast Cancer Symposium, vol. 72. San Antonio, TX: Cancer Research; 2012. p. S1-1.