Estrogen switches pure mucinous breast cancer to invasive lobular carcinoma with mucinous features

Breast Cancer Research and Treatment

Volumn 137, Issue 2, 2013, Pages 431-448

  Jambal, Purevsuren ^a   Badtke, Melanie M ^a   Harrell, J Chuck ^b   Borges, Virginia F ^a   Post, Miriam D ^a   Sollender, Grace E ^a   Spillman, Monique A ^a   Horwitz, Kathryn B ^a   Jacobsen, Britta M ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Estrogen; Hormone receptors; Invasive lobular carcinoma; Mucinous breast cancer; Xenografts

Indexed keywords

ANDROGEN RECEPTOR; ESTROGEN; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR; ESTRADIOL; TAMOXIFEN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST CARCINOMA; CANCER CELL CULTURE; CARCINOGENICITY; CASE REPORT; CELL PROLIFERATION; CHROMOSOME ANALYSIS; CONTROLLED STUDY; FEMALE; HORMONAL REGULATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KARYOTYPING; MOUSE; MUCINOUS BREAST CANCER; NONHUMAN; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR XENOGRAFT; AGED; ANIMAL; BREAST TUMOR; DRUG EFFECT; DRUG SCREENING; GENETICS; LUNG CARCINOMA; METABOLISM; NEOPLASM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

AGED; ANIMALS; BREAST NEOPLASMS; CARCINOMA, LOBULAR; CELL LINE, TUMOR; CELL PROLIFERATION; ESTRADIOL; ESTROGENS; FEMALE; HUMANS; KARYOTYPING; MICE; MICE, NUDE; NEOPLASMS, CYSTIC, MUCINOUS, AND SEROUS; TAMOXIFEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MLCS; MLOWN;

EID: 84880586138     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-012-2377-x     Document Type: Article

References (82)

1. Tavassoli FA, Devilee P (eds) (2003) World Health Organization Classification of Tumours. Pathology and genetics of tumours of the breast and female genital organs. IARC Press, Lyon
2. Henson D, Tarone R (1979) A study of lobular carcinoma of the breast based on the third national cancer survey in The United States of America. Tumori 65(2):133-142
3. Dixon JM, Anderson TJ, Page DL, Lee D, Duffy SW (1982) Infiltrating lobular carcinoma of the breast. Histopathology 6(2):149-161
4. Martinez V, Azzopardi JG (1979) Invasive lobular carcinoma of the breast: incidence and variants. Histopathology 3(6):467-488
5. Steinbrecher JS, Silverberg SG (1976) Signet-ring cell carcinoma of the breast. The mucinous variant of infiltrating lobular carcinoma? Cancer 37(2):828-840
6. Li CI, Anderson BO, Porter P, Holt SK, Daling JR, Moe RE (2000) Changing incidence rate of invasive lobular breast carcinoma among older women. Cancer 88(11):2561-2569
7. Li CI, Weiss NS, Stanford JL, Daling JR (2000) Hormone replacement therapy in relation to risk of lobular and ductal breast carcinoma in middle-aged women. Cancer 88(11):2570-2577
8. O'Connor IF, Shembekar MV, Shousha S (1998) Breast carcinoma developing in patients on hormone replacement therapy: a histological and immunohistological study. J Clin Pathol 51(12):935-938
9. Pestalozzi BC, Zahrieh D, Mallon E, Gusterson BA, Price KN, Gelber RD, Holmberg SB, Lindtner J, Snyder R, Thurlimann B, Murray E, Viale G, Castiglione-Gertsch M, Coates AS, Goldhirsch A (2008) 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 26(18):3006-3014. doi: 10.1200/JCO.2007.14.9336
10. Zhao H, Langerod A, Ji Y, Nowels KW, Nesland JM, Tibshirani R, Bukholm IK, Karesen R, Botstein D, Borresen-Dale AL, Jeffrey SS (2004) Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Mol Biol Cell 15(6):2523-2536. doi: 10.1091/mbc.E03-11-0786
11. Weigelt B, Geyer FC, Natrajan R, Lopez-Garcia MA, Ahmad AS, Savage K, Kreike B, Reis-Filho JS (2010) 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 220(1):45-57
12. Bertucci F, Orsetti B, Negre V, Finetti P, Rouge C, Ahomadegbe JC, Bibeau F, Mathieu MC, Treilleux I, Jacquemier J, Ursule L, Martinec A, Wang Q, Benard J, Puisieux A, Birnbaum D, Theillet C (2008) Lobular and ductal carcinomas of the breast have distinct genomic and expression profiles. Oncogene 27(40):5359-5372. doi: 10.1038/onc.2008.158
13. Turashvili G, Bouchal J, Baumforth K, Wei W, Dziechciarkova M, Ehrmann J, Klein J, Fridman E, Skarda J, Srovnal J, Hajduch M, Murray P, Kolar Z (2007) Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis. BMC Cancer 7:55. doi: 10.1186/1471-2407-7-55
14. Turashvili G, Bouchalova K, Bouchal J, Kolar Z (2007) Expression of E-cadherin and c-erbB-2/HER-2/neu oncoprotein in high-grade breast cancer. Cesk Pathol 43(3):87-92
15. Ellis IO, Pinder SE, Bobrow L et al (2005) Classifying invasive carcinomas Pathology reporting of breast disease, vol. no 58. NHSBSP publications: The Royal College of Pathologists, Sheffield, pp 61-69
16. Rosen PP (2009) Rosen's breast pathology, 3rd edn. Wolters Kluwer/Lippincott Williams & Wilkins, Philadelphia
17. Yu J, Bhargava R, Dabbs DJ (2010) Invasive lobular carcinoma with extracellular mucin production and HER-2 overexpression: a case report and further case studies. Diagn Pathol 5:36
18. Rosa M, Mohammadi A, Masood S (2009) Lobular carcinoma of the breast with extracellular mucin: new variant of mucin-producing carcinomas? Pathol Int 59(6):405-409. doi: 10.1111/j.1440-1827.2009.02385.x
19. Haltas H, Bayrak R, Yenidunya S, Kosehan D, Sen M, Akin K (2012) Invasive lobular carcinoma with extracellular mucin as a distinct variant of lobular carcinoma: a case report. Diagn Pathol 7(1):91. doi: 10.1186/1746-1596-7-91
20. Breslow A, Brancaccio ME (1976) Intracellular mucin production by lobular breast carcinoma cells. Arch Pathol Lab Med 100(11):620-621
21. Gad A, Azzopardi JG (1975) Lobular carcinoma of the breast: a special variant of mucin-secreting carcinoma. J Clin Pathol 28(9):711-716
22. Frost AR, Terahata S, Yeh IT, Siegel RS, Overmoyer B, Silverberg SG (1995) The significance of signet ring cells in infiltrating lobular carcinoma of the breast. Arch Pathol Lab Med 119(1):64-68
23. Merino MJ, Livolsi VA (1981) Signet ring carcinoma of the female breast: a clinicopathologic analysis of 24 cases. Cancer 48(8):1830-1837
24. Hull MT, Seo IS, Battersby JS, Csicsko JF (1980) Signet-ring cell carcinoma of the breast: a clinicopathologic study of 24 cases. Am J Clin Pathol 73(1):31-35
25. Rosen PP, Lesser ML, Kinne DW (1985) Breast carcinoma at the extremes of age: a comparison of patients younger than 35 years and older than 75 years. J Surg Oncol 28(2):90-96
26. Diab SG, Clark GM, Osborne CK, Libby A, Allred DC, Elledge RM (1999) Tumor characteristics and clinical outcome of tubular and mucinous breast carcinomas. J Clin Oncol 17(5):1442-1448
27. Weigelt B, Horlings HM, Kreike B, Hayes MM, Hauptmann M, Wessels LF, de Jong D, Van de Vijver MJ, Van't Veer LJ, Peterse JL (2008) Refinement of breast cancer classification by molecular characterization of histological special types. J Pathol 216(2):141-150
28. Adsay NV, Merati K, Nassar H, Shia J, Sarkar F, Pierson CR, Cheng JD, Visscher DW, Hruban RH, Klimstra DS (2003) Pathogenesis of colloid (pure mucinous) carcinoma of exocrine organs: coupling of gel-forming mucin (MUC2) production with altered cell polarity and abnormal cell-stroma interaction may be the key factor in the morphogenesis and indolent behavior of colloid carcinoma in the breast and pancreas. Am J Surg Pathol 27(5):571-578
29. Zotter S, Hageman PC, Lossnitzer A, van den Tweel J, Hilkens J, Mooi WJ, Hilgers J (1988) Monoclonal antibodies to epithelial sialomucins recognize epitopes at different cellular sites in adenolymphomas of the parotid gland. Int J Cancer Suppl 3:38-44
30. Kato N, Endo Y, Tamura G, Katayama Y, Motoyama T (1999) Mucinous carcinoma of the breast: a multifaceted study with special reference to histogenesis and neuroendocrine differentiation. Pathol Int 49(11):947-955
31. Chu JS, Chang KJ (1999) Mucin expression in mucinous carcinoma and other invasive carcinomas of the breast. Cancer Lett 142(1):121-127
32. Fentiman IS, Millis RR, Smith P, Ellul JP, Lampejo O (1997) Mucoid breast carcinomas: histology and prognosis. Br J Cancer 75(7):1061-1065
33. Andre S, Cunha F, Bernardo M, Meneses e Sousa J, Cortez F, Soares J (1995) Mucinous carcinoma of the breast: a pathologic study of 82 cases. J Surg Oncol 58(3):162-167
34. Paramo JC, Wilson C, Velarde D, Giraldo J, Poppiti RJ, Mesko TW (2002) Pure mucinous carcinoma of the breast: is axillary staging necessary? Ann Surg Oncol 9(2):161-164
35. Norris HJ, Taylor HB (1965) Prognosis of mucinous (gelatinous) carcinoma of the breast. Cancer 18:879-885
36. Toikkanen S, Kujari H (1989) Pure and mixed mucinous carcinomas of the breast: a clinicopathologic analysis of 61 cases with long-term follow-up. Hum Pathol 20(8):758-764
37. Silverberg SG, Kay S, Chitale AR, Levitt SH (1971) Colloid carcinoma of the breast. Am J Clin Pathol 55(3):355-363
38. Rasmussen BB (1985) Human mucinous breast carcinomas and their lymph node metastases. A histological review of 247 cases. Pathol Res Pract 180(4):377-382
39. Gadre SA, Perkins GH, Sahin AA, Sneige N, Deavers MT, Middleton LP (2008) Neovascularization in mucinous ductal carcinoma in situ suggests an alternative pathway for invasion. Histopathology 53(5):545-553
40. Ross DT, Scherf U, Eisen MB, Perou CM, Rees C, Spellman P, Iyer V, Jeffrey SS, Van de Rijn M, Waltham M, Pergamenschikov A, Lee JC, Lashkari D, Shalon D, Myers TG, Weinstein JN, Botstein D, Brown PO (2000) Systematic variation in gene expression patterns in human cancer cell lines. Nat Genet 24(3):227-235
41. Jacobsen BM, Harrell JC, Jedlicka P, Borges VF, Varella-Garcia M, Horwitz KB (2006) Spontaneous fusion with, and transformation of mouse stroma by, malignant human breast cancer epithelium. Cancer Res 66(16):8274-8279
42. Pinto MP, Badtke MM, Dudevoir ML, Harrell JC, Jacobsen BM, Horwitz KB (2010) Vascular endothelial growth factor secreted by activated stroma enhances angiogenesis and hormone-independent growth of estrogen receptor-positive breast cancer. Cancer Res 70(7):2655-2664. doi: 10.1158/0008-5472.CAN-09-4373
43. Kabos P, Haughian JM, Wang X, Dye WW, Finlayson C, Elias A, Horwitz KB, Sartorius CA (2011) Cytokeratin 5 positive cells represent a steroid receptor negative and therapy resistant subpopulation in luminal breast cancers. Breast Cancer Res Treat 128(1):45-55. doi: 10.1007/s10549-010-1078-6
44. van Bokhoven A, Caires A, Maria MD, Schulte AP, Lucia MS, Nordeen SK, Miller GJ, Varella-Garcia M (2003) Spectral karyotype (SKY) analysis of human prostate carcinoma cell lines. Prostate 57(3):226-244
45. Richer JK, Jacobsen BM, Manning NG, Abel MG, Wolf DM, Horwitz KB (2002) Differential gene regulation by the two progesterone receptor isoforms in human breast cancer cells. J Biol Chem 277(7):5209-5218
46. Jacobsen BM, Jambal P, Schittone SA, Horwitz KB (2009) ALU repeats in promoters are position-dependent co-response elements (coRE) that enhance or repress transcription by dimeric and monomeric progesterone receptors. Mol Endocrinol 23(7):989-1000. doi: 10.1210/me.2009-0048
47. Toikkanen S, Eerola E, Ekfors TO (1988) Pure and mixed mucinous breast carcinomas: DNA stemline and prognosis. J Clin Pathol 41(3):300-303
48. Weigelt B, Geyer FC, Horlings HM, Kreike B, Halfwerk H, Reis-Filho JS (2009) Mucinous and neuroendocrine breast carcinomas are transcriptionally distinct from invasive ductal carcinomas of no special type. Mod Pathol 22(11):1401-1414
49. Ko CD, Kim JS, Ko BG, Son BH, Kang HJ, Yoon HS, Cho EY, Gong G, Ahn SH (2003) The meaning of the c-kit proto-oncogene product in malignant transformation in human mammary epithelium. Clin Exp Metastasis 20(7):593-597
50. Jones C, Mackay A, Grigoriadis A, Cossu A, Reis-Filho JS, Fulford L, Dexter T, Davies S, Bulmer K, Ford E, Parry S, Budroni M, Palmieri G, Neville AM, O'Hare MJ, Lakhani SR (2004) Expression profiling of purified normal human luminal and myoepithelial breast cells: identification of novel prognostic markers for breast cancer. Cancer Res 64(9):3037-3045
51. Wan Y, Nordeen SK (2002) Overlapping but distinct gene regulation profiles by glucocorticoids and progestins in human breast cancer cells. Mol Endocrinol 16(6):1204-1214
52. Ghatge RP, Jacobsen BM, Schittone SA, Horwitz KB (2005) The progestational and androgenic properties of medroxyprogesterone acetate: gene regulatory overlap with dihydrotestosterone in breast cancer cells. Breast Cancer Res 7(6):R1036-R1050
53. Karey KP, Sirbasku DA (1988) Differential responsiveness of human breast cancer cell lines MCF-7 and T47D to growth factors and 17 beta-estradiol. Cancer Res 48(14):4083-4092
54. Sartorius CA, Shen T, Horwitz KB (2003) Progesterone receptors A and B differentially affect the growth of estrogen-dependent human breast tumor xenografts. Breast Cancer Res Treat 79(3):287-299
55. Waaseth M, Bakken K, Dumeaux V, Olsen KS, Rylander C, Figenschau Y, Lund E (2008) Hormone replacement therapy use and plasma levels of sex hormones in the Norwegian Women and Cancer postgenome cohort - a cross-sectional analysis. BMC Womens Health 8:1. doi: 10.1186/1472-6874-8-1
56. Molavi D, Argani P (2008) Distinguishing benign dissecting mucin (stromal mucin pools) from invasive mucinous carcinoma. Adv Anat Pathol 15(1):1-17
57. Wilson TE, Helvie MA, Oberman HA, Joynt LK (1995) Pure and mixed mucinous carcinoma of the breast: pathologic basis for differences in mammographic appearance. AJR Am J Roentgenol 165(2):285-289
58. Dabbs DJ, Bhargava R, Chivukula M (2007) Lobular versus ductal breast neoplasms: the diagnostic utility of p120 catenin. Am J Surg Pathol 31(3):427-437. doi: 10.1097/01.pas.0000213386.63160.3f
59. Capella C, Eusebi V, Mann B, Azzopardi JG (1980) Endocrine differentiation in mucoid carcinoma of the breast. Histopathology 4(6):613-630
60. Kehr EL, Jorns JM, Ang D, Warrick A, Neff T, Degnin M, Lewis R, Beadling C, Corless CL, Troxell ML (2012) Mucinous breast carcinomas lack PIK3CA and AKT1 mutations. Hum Pathol. doi: 10.1016/j.humpath.2012.03.012
61. Eltorky M, Hall JC, Osborne PT, el Zeky F (1994) Signet-ring cell variant of invasive lobular carcinoma of the breast. A clinicopathologic study of 11 cases. Arch Pathol Lab Med 118(3):245-248
62. Raju U, Ma CK, Shaw A (1993) Signet ring variant of lobular carcinoma of the breast: a clinicopathologic and immunohistochemical study. Mod Pathol 6(5):516-520
63. Harris M, Vasudev KS, Anfield C, Wells S (1978) Mucin-producing carcinomas of the breast: ultrastructural observations. Histopathology 2(3):177-188
64. Chu PG, Weiss LM (2004) Immunohistochemical characterization of signet-ring cell carcinomas of the stomach, breast, and colon. Am J Clin Pathol 121(6):884-892. doi: 10.1309/A09E-RYMF-R64N-ERDW
65. Foote FW, Stewart FW (1941) Lobular carcinoma in situ: a rare form of mammary cancer. Am J Pathol 17(4):491-496.3
66. Allred DC, Mohsin SK, Fuqua SA (2001) Histological and biological evolution of human premalignant breast disease. Endocr Relat Cancer 8(1):47-61
67. Khilko N, Wang J, Wei B, Hicks DG, Tang P (2010) Invasive lobular carcinomas do not express basal cytokeratin markers CK5/6, CK14 and CK17. Breast Cancer (Auckl) 4:49-55. doi: 10.4137/BCBCR.S5037
68. Huiping C, Sigurgeirsdottir JR, Jonasson JG, Eiriksdottir G, Johannsdottir JT, Egilsson V, Ingvarsson S (1999) Chromosome alterations and E-cadherin gene mutations in human lobular breast cancer. Br J Cancer 81(7):1103-1110. doi: 10.1038/sj.bjc.6690815
69. Di Saverio S, Gutierrez J, Avisar E (2008) A retrospective review with long term follow up of 11,400 cases of pure mucinous breast carcinoma. Breast Cancer Res Treat 111(3):541-547
70. Clayton F (1986) Pure mucinous carcinomas of breast: morphologic features and prognostic correlates. Hum Pathol 17(1):34-38
71. Komenaka IK, El-Tamer MB, Troxel A, Hamele-Bena D, Joseph KA, Horowitz E, Ditkoff BA, Schnabel FR (2004) Pure mucinous carcinoma of the breast. Am J Surg 187(4):528-532
72. Reeves GK, Beral V, Green J, Gathani T, Bull D, Million Women Study C (2006) Hormonal therapy for menopause and breast-cancer risk by histological type: a cohort study and meta-analysis. Lancet Oncol 7(11):910-918
73. Shousha S, Coady AT, Stamp T, James KR, Alaghband-Zadeh J (1989) Oestrogen receptors in mucinous carcinoma of the breast: an immunohistological study using paraffin wax sections. J Clin Pathol 42(9):902-905
74. Prat A, Ellis MJ, Perou CM (2012) Practical implications of gene-expression-based assays for breast oncologists. Nat Rev Clin Oncol 9(1):48-57. doi: 10.1038/nrclinonc.2011.178
75. Acs G, Esposito NN, Kiluk J, Loftus L, Laronga C (2012) A mitotically active, cellular tumor stroma and/or inflammatory cells associated with tumor cells may contribute to intermediate or high Oncotype DX recurrence scores in low-grade invasive breast carcinomas. Mod Pathol 25(4):556-566. doi: 10.1038/modpathol.2011.194
76. Kounalakis N, Diamond J, Rusthoven K, Horn W, Jindal S, Wisell J, Klein CE, Elias A, Finlayson C, Borges VF (2011) Diagnosis of invasive lobular carcinoma in a young woman presenting with pleomorphic lobular carcinoma in situ on core biopsy. Oncology (Williston Park) 25(4):351-356
77. Cho LC, Hsu YH (2008) Expression of androgen, estrogen and progesterone receptors in mucinous carcinoma of the breast. Kaohsiung J Med Sci 24(5):227-232. doi: 10.1016/S1607-551X(08)70146-3
78. Melamed MR, Robbins GF, Foote FW Jr (1961) Prognostic significance of gelatinous mammary carcinoma. Cancer 14:699-704
79. Komaki K, Sakamoto G, Sugano H, Morimoto T, Monden Y (1988) Mucinous carcinoma of the breast in Japan. A prognostic analysis based on morphologic features. Cancer 61(5):989-996
80. Stanley MW, Tani EM, Skoog L (1989) Mucinous breast carcinoma and mixed mucinous-infiltrating ductal carcinoma: a comparative cytologic study. Diagn Cytopathol 5(2):134-138
81. Rosen PP, Wang T-Y (1980) Colloid carcinoma of the breast. Analysis of 64 patients with long term followup. Am J Clin Pathol 73:304
82. Pusztai L, Sotiriou C, Buchholz TA, Meric F, Symmans WF, Esteva FJ, Sahin A, Liu ET, Hortobagi GN (2003) Molecular profiles of invasive mucinous and ductal carcinomas of the breast: a molecular case study. Cancer Genet Cytogenet 141(2):148-153