The -synuclein Expression as a Prognostic Factor in Breast Cancer 115 서는거의알려져있지않다. 유방암특이유전자로밝혀진 breast cancer specific gene 1 (BCSG1) 은유방암의 cdna libra

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1 Journal of Breast Cancer ISSN J Breast Cancer 2007; June 10 (2): ORIGNAL ARTICLE 유방암에서 -Synuclein 과발현의예후인자로서유용성및 HER-2/neu 유전자증폭과연관성 김성래ㆍ최원혁ㆍ박준호ㆍ남은숙 1 ㆍ조성진 1 ㆍ박찬흔 한림대학교의과대학외과학교실, 1 병리학교실 The -Synuclein Expression in Breast Cancer and its Correlation with the Expression of the HER-2/neu Gene Seong Rae Kim, Won Hyuk Choi, Jun Ho Park, Eun Sook Nam 1, Seong Jin Cho 1, Chan Heun Park Departments of Surgery and 1 Pathology, Hallym University College of Medicine, Seoul, Korea Purpose: Synuclein has been identified as an important neuroprotein for developing pathologic deposits in Alzheimer s and Parkinson s disease patients. -synuclein is also known as a breast cancer-specific gene 1 thats s not found in normal breast tissues but it has been reported to be overexpressed in breast cancer, ovarian cancer and other tumors. To evaluate the availability of -synuclein expression as a prognostic factor for infiltrative breast cancer, we analyzed its correlation with the clinical parameters and the HER-2/neu gene expression. Methods: Two hundred fiffty samples of breast cancer tissues embedded in paraffin and that were obtained from the infiltrative breast cancer patients who were operated in our institution from January 1995 to December 2000 were analyzed with employing the tissue microarray technique. The expression of -synuclein was studied with immunohistochemistry and with using -synulcein antibodies. One hundred thirty one cases that showed favorable staining were selected and studied retrospectively. Results: Fiffty five% (71/131) of the patients showed -synuclein overexpression. The histopathological findings that significantly correlated with -synuclein overexpression were the number of metastatic lymph nodes (p<0.01) and the cancer stage (p<0.01). Using the same tissue mircoarray, the HER-2/neu gene expression and -synuclein expression also showed statistically significant correlation (p=0.04). Conclusion: -synuclein overexpression showed significant correaltion with lymph node metastasis and cancer stage. It also showed significant relevance with the HER-2/neu gene expression, and that is already known to be a prognostic factor for breast cancer. Therefore -synuclein may be a useful prognostic factor for infiltrative breast cancer and further studies on the its correlation with survival, local recurrence, and distant metastasis should be conducted (J Breast Cancer 2007;10:114-9) Key Words : Invasive ductal carcinoma, -synuclein, HER-2/neu, Immunohistochemistry 중심단어 : 침윤성유방관암종, -synuclein, HER-2/neu, 면역조직화학검사 서 론 책임저자 : 박찬흔 서울시강동구길 1 동 445, 한림대학교강동성심병원외과 Tel: , Fax: hhh@hallym.or.kr 접수일 : 2006 년 10 월 26 일게재승인일 : 2007 년 5 월 31 일 Synucleins 는 3 개의단백질, -synuclein (SNCA), -synuclein (SNCB), -synuclein (SNCG) 으로이루어진작은크기의단백질군이다.(1, 2) -synuclein 유전자는 10q23에위치하며 5개의 coding exon으로이루어져있고 1 kb 의 mrna로전사된다. 인간의 -synuclein은 127개의아미노산으로이루어져있다.(3) Synucleins가 presynaptic terminal에서풍부하게발현되고, 알츠하이머병의 amyloid plaque 형성, 파킨슨병의 Lewy body 형성과관련이있지만 (4) 세포내정상기능에대해 114

2 The -synuclein Expression as a Prognostic Factor in Breast Cancer 115 서는거의알려져있지않다. 유방암특이유전자로밝혀진 breast cancer specific gene 1 (BCSG1) 은유방암의 cdna library에서높은빈도로발현되고정상유방조직의 cdna library에서는거의발현되지않는다.(5) BCSG1은기존의알려진다른성장인자나암유전자와상동성이없고신경단백인 synucleins와염기서열상동성을나타냈다 (SNCA와 54%, SNCB와 56%).(6) BCSG1 동정이후 synuclein(3) 과 persyn(7) 이뇌 genomic library와뇌 cdna library로부터각각동정되었고, 세개의단백질은동일한단백질로밝혀졌다. 이후 BSCG1은 -synuclein로명명하게되었다. Ji 등 (5) 은 -synuclein이유방암에서비정상적으로발현되는것을최초로발견하였다. 그들은 Northern blot과 in situ hybridization을이용하여악성유방암에서높은빈도로 -synuclein mrna가발현되고양성유방종양혹은정상유방조직에서는 -synuclein mrna가거의발현되지않는것을밝혀내었다. -synuclein의과발현이암종의발생및성장에미치는영향에대해현재까지알려진것은실험적으로세포의운동성과침윤성을증가시키고 (in vitro) 생체내에서전이를촉진 (in vivo) 시키며항암제유발세포자살에저항성을가지게한다는것이다.(8) Synucleins의과발현은난소암의발생과도관련이있는것으로알려져있다.(9) 최근 -synuclein이유방암과난소암뿐만아니라다른여러암종 ( 간암, 식도암, 대장암, 위암, 폐암, 전립선암, 자궁경부암 ) 에서도과발현되며이들암종의병기가높을수록그발현빈도가높다는결과가보고되었다.(10) 이전의연구들을통해유방암에서 -synuclein이유방암의병기에특이적으로발현한다는사실은 Western 분석 (9), RT-PCR 분석 (11) 을통해확인되었다. 본저자들은침윤성유방암에서면역조직화학염색을이용하여조직병리학적소견과 -synuclein의과발현여부및환자의임상병기와의연관성을조사하였다. 또한유방암의예후인자인 HER-2/neu 유전자증폭과 -synuclein의과발현의상관성을조사하여 -synuclein 과발현의예후인자로서의유용성을평가하고자하였다. 방법 였고, 에스트로겐수용체와프로게스테론수용체는면역조직화학검사로시행된기존의결과를이용하였다. 이중염색상태가양호한 131 명을대상으로의무기록을통한후향적연구를시행하였다. 2. 연구방법 1) -synuclein에대한면역조직화학염색면역조직화학연구는 goat anti-human -synuclein polyclonal antibody (clone C-20, 1:200, Santa Cruz Biotechnology, CA, USA) 을 1차항체로사용하여 avidin-biotin complex method 로시행하였다. 포르말린에고정된파라핀포매조직의조직미세배열을 4 m 두께로절제한면역조직화학염색용슬라이드에부착시킨후 xylene을이용하여탈파라핀화하고알코올로수세하였다. 슬라이드를 10 mm citrate 완충액에담근후항원복구를위해전자렌지에서 5분간 2회가열하였다. 내인성과산화효소는 0.3% 과산화수소로 20 분이상억제시킨후켰다. 슬라이드는일차항체와함께 phosphate buffered saline과 1% bovine serum albumin에 4 에서하룻밤동안반응시켰다. 이차항체로 anti-goat biotinylated antibody를실온에서 20 분간반응시킨후 3-3 -diaminobendizine-tetrachloride (Biogenex, San Ramon, CA, USA) 를발색제로사용한 LSAB kit (DAKO, Carpinteria, CA, USA) 를사용하였다. 이후슬라이드는 Meyer s hematoxyline을이용하여대조염색을하였다. 음성대조군은일차항체대신식염수를이용하여반응시킨것을이용하였다. 면역염색된슬라이드는양성반응을보이는세포의비례점수 (proportion score) 와염색점수 (intensity score) 를측정하여검사하였다. 비례점수는면역반응성세포가관찰되지않을때 0, 면역반응성세포가 5% 미만, 5-10%, 10-40%, 40-70%, 70% 이상일때각각 1, 2, 3, 4, 5로등급을나누었다. 염색점수는면역반응성이없을때 0, 염색강도가약, 중간, 강일때각각 1, 2, 3으로등급을나누었다. 면역반응성의최종측정치는비례점수와염색점수의합이 4 미만일때음성, 4-8 사이일때양성으로평가하였다 (Fig 1). 1. 연구대상 1995년 1월부터 2000년 12 월까지본원에서침윤성유방암진단하에수술을시행한환자들의원발성암조직중파라핀포매조직의보관상태가양호한 250 예를대상으로조직미세배열을시행하였다. -synuclein의과발현여부는 -synuclein에대한항체를이용한면역조직화학염색으로측정하였으며, 동일한조직미세배열을이용하여 HER-2/neu 유전자증폭은형광제자리부합화 (fluorescence in situ hybridization, FISH) 로확인하 2) HER-2/neu 유전자증폭측정을위한 FISH HER-2/neu 유전자증폭은 FISH를이용하여측정하였다. 녹색의 chromosome 17 centromeric probe와오렌지색의 HER- 2 probe (17q11.2-q12) 를이용하여 2-color FISH (Vysis inc., Downers Grove, IL, USA) 를시행하였다. 모든사례에서오렌지신호가녹색신호에비해 2배이상인경우에증폭된것으로판독하였다.

3 116 Seong Rae Kim, et al. A B Fig 1. Immunohistochemistry of -synuclein (A) non-expression of -synuclein (B) expression of -synuclein (brown color). 3) 통계학적분석 SPSS 10.1을이용하여조직병리학적소견과 -synuclein의과발현여부및환자의임상병기와의연관성을 chi-square 검정하였으며통계학적유의성은 p<0.05를기준으로하였다. 결과환자들의평균연령은 50.0±11.5세였다. 조직병리학적소견상유방암의병기는 I기 27 예 (20.6%), IIA기 58 예 (44.8%), IIB기 14예 (10.7%), IIIA기 28 예 (21.4%), IIIB기 2예 (1.5%), IV기는 2 예 (1.5%) 였다. 에스트로겐수용체와프로게스테론수용체의양성여부는 117 예에서관찰이가능했다. 에스트로겐수용체는 117 예중 50 예 (43.1%) 에서양성이었고, 프로게스테론수용체는 117 예중 37예 (31.9%) 에서양성이었다. HER-2/neu 유전자증폭은 131예중 36 예 (27.5%) 에서관찰되었다. 대상환자 (n=131) 중 55.0 % (72/131) 에서 synuclein 과발현소견이관찰되었다 (Table 1). 조직병리학적소견에따른 -synuclein의과발현의결과는다음과같았다. 암종의크기가 2 cm 미만인경우가 35 예였고이중 19예 (54.3%) 에서 -synuclein이과발현되었으며, 암종의크기가 2-5 cm인경우는 85예였고이중 47 예 (55.3%) 에서 - synuclein이과발현되었다. 암종의크기가 5 cm 이상인경우는 11예였고이중 6예 (54.5%) 에서 -synuclein이과발현되었다. 암종의크기에따른 -synuclein의과발현여부는통계적으로유의한차이가없었다 (Table 2). 림프절전이상태에따라 N0가 81예였고이중 35예 (43.2%) 에서 -synuclein이과발현되었으 Table 1. Clinicopathologic findings of 131 invasive ductal carcinomas No. (%) Pathologic tumor T1 35 (26.7) T2 85 (64.9) T3 11 (8.4) Axillary LN N0 81 (61.9) N1 17 (13.0) N2 33 (25.3) Stage I 27 (20.6) II 72 (55.0) III 30 (22.9) IV 2 (1.5) ER status (n=116) Negative 66 (56.9) Positive 50 (43.1) PR status (n=116) Negative 79 (68.1) Positive 37 (31.9) HER-2/neu Not amplified 95 (72.5) Amplified 36 (27.5) LN=lymph node; ER=estrogen receptor; PR=progesterone receptor. 며, N1 은 17예였고이중 11 예 (64.7%) 에서 -synuclein이과발현되었다. N2 가 33 예였고이중 26 예 (78.8%) 에서 -synuclein 이과발현되었다. 림프절전이의수가증가할수록통계적으로유의하게 (p=0.002) -synuclein이과발현되었다 (Table 2). 암종의병기에따른 -synuclein의과발현의결과는다음과같았다.

4 The -synuclein Expression as a Prognostic Factor in Breast Cancer 117 Table 2. -synuclein expression according to the clinicopathological factors Table 3. Correlation between -synuclein expression and HER- 2/neu amplification -synuclein Not expressed (%) 59 (45.0) Expressed (%) 72 (55.0) p- value -synuclein Not expressed (%) Expressed (%) 59 (45.0) 72 (55.0) p- value Pathologic tumor T1 (n=35) 16 (45.8) 19 (54.3) T2 (n=85) 38 (44.7) 47 (55.3) T3 (n=11) 5 (45.5) 6 (54.5) 0.9 Axillary LN N0 (n=81) 46 (56.8) 35 (43.2) N1 (n=17) 6 (35.3) 11 (64.7) N2 (n=33) 7 (21.2) 26 (78.8) Stage I/II (n=99) 51 (51.5) 48 (48.5) III/IV (n=32) 8 (25.0) 24 (75.0) ER status Negative (n=66) 27 (40.9) 39 (59.1) Positive (n=50) 22 (44.0) 28 (56.0) 0.7 PR status Negative (n=79) 36 (45.6) 43 (54.4) Positive (n=37) 17 (45.9) 20 (54.1) 0.9 LN=lymph node; ER=estrogen receptor; PR=progesterone receptor. I/II 기에서 99 예중 48 예 (48.5%) 가 -synuclein 의과발현을보 였다. III/IV기에서 32예중 24예 (78.8%) 에서 -synuclein의과발현을보였다. I/II기에비해 III/IV기에서통계적으로유의하게 (p=0.009) -synuclein이과발현되는것을확인하였다 (Table 2). 에스트로겐수용체양성인 50 예중 28 예 (56.0%) 에서 -synuclein이과발현되었으며프로게스테론수용체양성인 37 예에서는 20예 (54.1%) 에서 -synuclein이과발현되었다. 에스트로겐수용체와프로게스테론수용체가양성인경우와 -synuclein 의과발현은통계적으로상관관계가없었다 (p>0.05) (Table 2). HER-2/neu 유전자가과발현이되지않은 95 예중 47 예 (49.5 %) 에서 -synuclein이과발현되었으나, HER-2/neu 유전자가과발현된 36 예중에서는 25 예 (69.5%) 에서 -synuclein이과발현되었다. HER-2/neu 유전자의과발현과 -synuclein의과발현이통계적으로유의한상관관계 (p=0.04) 가있음을확인할수있었다 (Table 3). 고 유방암의발생및진행은다양한유전적변화에의한질적그리고양적인각각의유전자발현의변이에의해이루어진다. 이러한변이에따른유전자의산물과세포내기능의변화는세포의정상대사를방해하고암형성을초래한다. 암종에서과발현혹은미발현되는유전자를동정하고생물학적기능을밝히는것은악성변 찰 HER-2/neu Not amplified (%) 48 (50.5) 47 (49.5) 95 (72.5) Amplified (%) 11 (30.6) 25 (69.5) (27.5) 화의과정을이해하는데중요하다. Synucleins 단백질군중 - synuclein의 Western 분석을통해 -synuclein이정상유방조직과 I/II기유관상피암에서발현되지않고 III/IV기유관상피암의 70% 에서발현된다는연구결과가보고된후 (9) 이러한사실을뒷받침하는많은연구들이시행되었다. Ninkina 등 (7) 은 Northern blotting과 Western blotting을이용하여유방암과유방암세포주에서 -synuclein이발현되고정상유방조직에서는 -synuclein이발현되지않는다는것을확인하였다. Liu 등 (10) 은 79 개임상례의 RT-PCR 분석을통해 -synuclein의발현이유방암의병기에특이적이라고보고하였다. 본연구는면역조직화학염색을통해 -synuclein의과발현을관찰하였다. 본연구에서암종의크기와 -synuclein의과발현은상관관계가없었지만액와림프절전이상태와 -synuclein 의과발현은유의한상관관계가있었다. 또한 I/II기의유방암보다 III/IV기의유방암에서 -synuclein이과발현되는결과를얻었다. 기존의연구결과와같이 -synuclein의과발현이유방암의병기에특이적이라는사실을확인하였다. 침윤성유방암에서 -synuclein이높은빈도로발현되는것은 -synuclein이유방암의발생및진행에영향을미친다는것을시사한다. 그러나현재까지는 -synuclein이정상유방조직에서어떠한기능을갖고있는지또한유방암에어떻게영향을미치는지는거의밝혀지지않았다. Gupta 등 (11) 은 -synuclein 의 exon1에위치하는 CpG island의 hypomethylation에의해 -synuclein의발현이야기된다는것을보고하였다. Jiang 등 (12) 은 -synuclein이 ER- signaling을통하여 ligand 의존성세포의성장에영향을미치는것을발견하였다. 현재까지의연구결과 -synuclein은유방암의발생과진행에다음과같은역할을할것으로생각되고있다. 첫째, 암세포의이동성및전이의자극, 둘째, 항암제유발세포자살로부터암세포의보호이다.(13) 많은연구를통해유방암에대해다양한예후인자들이제시되었다. 이들중임상적으로폭넓게사용되는것들은 ER, PR, Proliferating Cell Nuclear Antigen (PCNA), HER-2/neu 등이다. HER-2/neu 과발현은유방암의악성도, 림프절전이등과

5 118 Seong Rae Kim, et al. 관련이있으며불량한예후와강력한상관관계가있다.(14-16) HER-2/neu의과발현을측정하는다양한검사법이있으며그방법마다상이한결과를보이고있다.(17-18) 최근에는대부분의연구실에서면역조직화학염색으로선별한후에 FISH를시행하거나단독으로시행하고있다.(19) HER-2/neu의과발현은현재재발성유방암및전이를동반한유방암에서 trastuzumab (Herceptin) 을이용한항암화학요법을결정하는데중요한역할을하고있다.(20) Wu 등 (8) 은 -synuclein의과발현이유방암의병기에특이적이라는사실을확인한연구에서 RT-PCR로확인한 -synuclein의과발현과면역조직화학염색으로확인한 HER- 2/neu의과발현이상관관계가없다는결과를보고하였다. 본연구에서는 -synuclein의과발현과 HER-2/neu의과발현의상관관계를알아보기위해동일한미세조직배열에서 -synuclein에대한면역조직화학염색과 HER-2/neu에대한 FISH 를시행하였고 -synuclein 의과발현과 HER-2/neu 의과발현이통계적으로유의하게상관관계가있음을확인하였다. -synuclein의과발현과 HER-2/neu의과발현에대한본연구와 Wu 등의보고가상이한결과를보였고검사법의차이에의해이러한결과가나왔는지등에대해추가적인연구가필요할것으로보인다. -synuclein의과발현이 HER-2/neu의과발현과관련이있다는본연구의결과는 -synuclein의과발현이유방암의불량한예후와연관이있을수있다는것을시사한다. 따라서 -synuclein의과발현이유방암에있어서예후인자로서유용성을가질것으로기대된다. 현재까지 -synuclein의과발현이유방암의예후에미치는영향에대한장기간의연구결과가보고되지않았으므로향후장기추적관찰을통하여 -synuclein이유방암의생존율, 국소재발및원격전이에미치는영향에대한연구가더필요할것이다. 결론아직까지국내에서보고되지않았던유방암에서의 -synuclein의과발현과임상병리학적소견을비교하여다음과같은결과를얻을수있었다. -synuclein이 55% 에서과발현되었고, 과발현과액와림프절전이및암종의병기와연관성이있었으며 HER-2/neu 유전자증폭과도연관성이있었다. -synuclein 의과발현이유방암의예후에밀접한영향을미칠것으로생각되며향후장기추적관찰을통한연구가필요할것으로생각된다. 참고문헌 1. Lavedan C. The synuclein family. Genome Res 1998;8: George JM. The synucleins. Genome Biol 2002;3:REVIEWS Lavedan C, Leroy E, Dehejia A, Buchholtz S, Dutra A, Nussbaum RL, et al. Identification, localization and characterization of the human -synuclein gene. Hum Genet 1998;103: Takeda A, Mallory M, Sundsmo M, Honer W, Hansen L, Masliah E. Abnormal accumulation of NACP/ -synuclein in neurodegenerative disorders. Am J Pathol 1998;152: Ji H, Liu YE, Jia T, Wang M, Liu J, Joseph BK, et al. Identification of a breast cancer-specific gene, SNCG, by direct differential complementary DNA sequencing. Cancer Res 1997;57: Clayton DF, George JM. The synucleins: a family of proteins involved in synaptic function, plasticity, neurodegeneration and disease. Trends Neurosci 1998;21: Ninkina N, Alimova-Kost M, Paterson J, Delaney L, Cohen B, Imreh S, et al. Organisation, expression and polymorphism of the human persyn gene. Hum Mol Genet 1998;7: Wu K, Weng Z, Tao Q, Lin G, Wu X, Qian H, et al. Stage-specific expression of breast cancer-specific gene gamma-synuclein. Cancer Epidemiol Biomarkers Prev 2003;12: Bruening W, Giasson BI, Klein-Szanto AJ, Lee VM, Trojanowski JQ, Godwin AK. Synucleins are expressed in the majority of breast and ovarian carcinomas and in preneoplastic lesions of the ovary. Cancer 2000;88: Liu H, Liu W, Wu Y, Zhou Y, Xue R, Luo C, et al. Loss of epigenetic control of synuclein-gamma gene as a molecular indicator of metastasis in a wide range of human cancers. Cancer Res 2005;65: Gupta A, Godwin AK, Vanderveer L, Lu A, Liu J. Hypomethylation of the synuclein gamma gene CpG island promotes its aberrant expression in breast carcinoma and ovarian carcinoma. Cancer Res 2003; 63: Jiang Y, Liu YE, Goldberg ID, Shi YE. Gamma synuclein, a novel heat-shock protein-associated haperone, stimulates ligand-dependent estrogen receptor alpha signaling and mammary tumorigenesis. Cancer Res 2004;64: Pan ZZ, Bruening W, Giasson BI, Lee VM, Godwin AK. -synuclein promotes cancer cell survival and inhibits stress- and chemotherapeutic drug-induced apoptosis by modulating MAPK athways. J Biol Chem 2002;277: Borg A, Tandon AK, Sigurdsson H, Clark GM, Ferno M, Fuqua SA, et al. HER-2/neu amplification predicts poor survival in node-positive breast cancer. Cancer Res 1990;50:

6 The -synuclein Expression as a Prognostic Factor in Breast Cancer Winstanley J, Cooke T, Murray GD, Platt-Higgins A, George WD, Holt S, et al. The long term prognostic significance of c-erb-2 in primary breast cancer. Br J Cancer 1991;63: Paterson MC, Dietrich KD, Danyluk J, Dono K, Kanai T, Mori Tl. Correlation between c-erb-2 amplification and risk of recurrent disease in node-negative breast cancer. Cancer Res 1991;51: Nichols DW, Wolff DJ, Self S, Metcalf JS, Jacobs D, Kneuper-Hall R, et al. A testing lgorithm for determination of HER2 status in patients with breast cancer. Ann Clin Lab Sci 2002;32: Wang S, Saboorian MH, Frenkel E, Hynan L, Gokaslan ST, Ashfaq R. Laboratory assessment of the status of Her-2/neu protein and oncogene in breast cancer specimens: comparison of immunohistochemistry assay with fluorescence in situ hybridisation assays. J Clin Pathol 2000;53: Ross JS, Fletcher JA, Linette GP, Stec J, Clark E, Ayers M, et al. The Her-2/neu gene and protein in breast cancer 2003: biomarker and target of therapy. Oncologist 2003;8: McKeage K, Perry CM. Trastuzumab: a review of its use in the treatment of metastatic breast cancer overexpressing HER2. Drugs 2002;62:

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