Kleer Lab


Peer-Reviewed Publications

Recent Publications (2013 - 2014)


Kim G, Ouzounova M, Quraishi AA, Davis A, Tawakkol N, Clouthier SG, Malik F, Paulson AK, D'Angelo RC, Korkaya S, Baker TL, Esen ES, Prat A, Liu S, Kleer CG, Thomas DG, Wicha MS, Korkaya H.SOCS3-mediated regulation of inflammatory cytokines in PTEN and p53 inactivated triple negative breast cancer model. Oncogene, in press.


Gonzalez, M.E., Moore, H.M., Li, X., Toy, K.A., Huang, W., Sabel, M.D., Kidwell, K., and Kleer, C.G. EZH2 expands breast stem cells through activation of NOTCH1 signaling. Proceedings of the National Academy of Sciences U.S.A. (PNAS), 2014 Feb 25;111(8):3098-103.


Chaffer, C.L., Marjanovic, N.D., Reinhardt, F., Kleer, C.G., Bell, G., Lee, T., D’Alessio, A.C., Young, R.A., Weinberg, R.A. Poised chromatin at the ZEB1 promoter enables cell plasticity and enhances tumorigenicity. Cell 154(1):61-74, 2013. PMID: 23827675.


Moore, H.M., Gonzalez, M.G., Toy, K.A., Cimino-Matthews, A., Argani, P., Kleer, C.G. EZH2 inhibition decreases p38 signaling and suppresses breast cancer motility and metastasis. Breast Cancer Res. Treat 138(3):741-52, 2013. PMCID: PMC3690767.


Arps, D., Kleer, C.G., Pang, J.C. Invasive ductal carcinoma with lobular features: A comparison study to invasive ductal and invasive lobular carcinomas of the breast. Breast Cancer Res. Treat 138(3):719-26, 2013. PMID: 23535842.


Anwar, T. and Kleer, C.G. Tissue based identification of stem cells and epithelial-to-mesenchymal transition in breast cancer. Human Pathology 44(8):1457-64, 2013. PMCID: PMC3715557.


Ithimakin, S., Day, K.C., Malik, F., Zen, Q., Dawsey, S,J,, Bersano-Begey, T.F., Quraishi, A.A., Ignatoski. K.W., Daignault, S., Davis, A., Hall, C.L., Palanisamy, N., Heath, A.N., Tawakkol, N., Luther, T.K., Clouthier, S.G., Chadwick, W.A., Day, M.L., Kleer, C.G., Thomas, D.G., Hayes, D.F., Korkaya, H., Wicha, M.S. HER2 drives luminal breast cancer stem cells in the absence of HER2 amplification: Implications for efficacy of adjuvant Trastuzumab. Cancer Res 1;73(5):1635-46, 2013. PMCID: PMC3600586.


Schwartz, T., Stark, A., Pang, J., Awuah, B., Kleer, C.G., Quayson, S., Kingman, S., Aitpillah, F., Abantanga, F., Jiagge, E., Oppong, J., Osei-Bonsu, E., Martin, I., Yan, X., Toy, K.A., Adjei, E., Wicha, M., and Newman, L.A.  Expression of ALDH1 as a Marker of Mammary Stem Cells in Benign and Malignant Breast Lesions of Ghanaian Women.  Cancer 119(3):488-494, 2013.  PMID: 22930220.


(2010 - 2012)


Pal, A., Huang, W., Toy, K.A., and Kleer, C.G. CCN6 knockdown disrupts acinar organization of breast cells in three-dimensional cultures via upregulation of Type III TGF-β receptor. Neoplasia 14, 1067-74, 2012. PMCID: PMC3514738.


Soliman A.S, Kleer. C.G., Mrad K., Karkouri M, Omar S, Khaled HM, Benider AL, Ayed FB, Eissa SS, Eissa MS, McSpadden EJ, Lo AC, Toy K, Kantor ED, Xiao Q, Hampton C, Merajver SD. Inflammatory breast cancer in North Africa: comparison of clinical and molecular epidemiologic characteristics of patients from Egypt, Tunisia, and Morocco. Breast Dis 33(4):159-69, 2012. PMID: 23001584.


Rosenthal DT, Zhang J, Bao L, Zhu L, Wu Z, Toy K, Kleer C.G., Merajver SD. RhoC impacts the metastatic potential and abundance of breast cancer stem cells. PLoS One 2012;7(7):e40979. Epub 2012 Jul 23. PMCID: PMC3402452.


Pal, A., Huang, W., Li, X., Toy, K.A., Nikolovska-Coleska, Z., and Kleer, C.G.  CCN6 modulates BMP signaling via the Smad-independent TAK1/p38 pathway, acting to suppress metastasis of breast cancer.  Cancer Research 72(18):4818-28, 2012. PMCID: PMC3505182.


Rungta, S. and Kleer, C.G. Metaplastic Carcinomas of the Breast: Diagnostic Challenges and New Translational Insights. Archives of Pathology and Laboratory Medicine 136(8):896-900, 2012. PMID: 22849737.


Pang, J., Toy, K.A., Griffith, K., Awuah, B., Quayson, S., Newman, L.A., and Kleer, C.G.  Invasive Breast Carcinomas in Ghana: High Frequency of High Grade, Basal-Like Histology and High EZH2 Expression.  Breast Cancer Research and Treatment, 135(1):59-66, 2012. PMID: 22527102.


Valiathan, R.R., Marco, M., Leitinger, B., Kleer, C.G., and Fridman, R. Discoidin Domain Receptor Tyrosine Kinases: New Players in Cancer Progression. Cancer Metastasis Reviews 31(1-2):295-321, 2012. PMCID: PMC3351584.


Wu Z-Q, Li X-Y, Hu CY, Ford M, Kleer, C.G. and Weiss SJ. Canonical Wnt signaling regulates Slug activity and links epithelial-mesenchymal transition with epigenetic Breast Cancer 1, Early Onset (BRCA1) repression. Proceedings of the National Academy of Sciences U.S.A. (PNAS) 109(41):16654-59, 2012. PMCID: PMC3478591.


Zhang Y, Toy KA, and Kleer C.G. Metaplastic Breast Carcinomas Are Enriched in Markers of Tumor-initiating Cells and Epithelial to Mesenchymal Transition. Modern Pathology 25(2):178-184, 2012. PMCID: PMC3360584.


Rosenthal, D.T., Iyer, H., Escudero, S., Bao, L., Wu, Z., Ventura, A.C., Kleer, C.G., Arruda, E.M., Garikipati, K., Merajver, S.D. P38(gamma)

Huang, W., Pal, A., and Kleer, C.G. On How CCN6 Suppresses Breast Cancer Growth and Invasion. Journal of Cell Communication and Signaling 6(1):5-10, 2012. PMCID: PMC3271195.

Alford, S.H., Toy, K.A., Merajver, S.D., and Kleer, C.G. Increased Risk for Distant Metastasis in Patients with Familial Early-stage Breast Cancer and High EZH2 Expression. Breast Cancer Research and Treatment, 132(2):429-437, 2012. PMCID: PMC3311223.Promotes Breast Cancer Cell Motility and Metastasis Through Regulation of RhoC GTPase, Cytoskeletal Architecture, and a Novel Leading Edge Behavior. Cancer Research 71(20):6338-6349, 2011. PMCID: PMC3193559.


Robinson, D.R., Kalyana-Sundaram, S., Wu, Y-M., Shankar, S., Cao, X.,  Ateeq, B., Asangani, I., Iyer, M.,  Maher, C., Grasso, C., Lonigro, R., Quist, M., Siddiqui, J., Mehra, R., Jing, X., Giordano, T.J., Sabel, M.S., Kleer, C.G., Palanisamy, N., Natrajan, R., Lambros, M., Reis-Filho, J., Kumar-Sinha, C., and Chinnaiyan, A.M. Functionally Recurrent Rearrangements of the MAST Kinase and Notch Gene Families in Breast Cancer. Nature Medicine 71(20):6338-6379, 2011. PMCID: PMC3233654.


Spencer B., Banerjee M., Omar S., Khaled H., Anwar N., Zaghloul M.S., Eissa S., Kleer C.G., Dey S., Merajver S.D., and Soliman A.S. Survival of Inflammatory Breast Cancer Patients Compared to Non-inflammatory Breast Cancer Patients in Egypt. The Breast Journal 17(5):545-547, 2011. PMID: 21827567.


Gonzalez, M.E., DuPrie, M.L., Krueger, H.M., Merajver, S.D., Ventura, A.C., Toy, K.A., and Kleer, C.G. Histone Methylatransferase EZH2 Induces Akt-dependent Genomic Instability and BRCA1 Inhibition in Breast Cancer. Cancer Research 71(6):2360-70, 2011. PMCID: PMC3071296.


Lorenzatti, G., Huang, W., Pal, A., Cabanillas, A.M*, and Kleer, C.G.* CCN6 (WISP3) Decreases ZEB1-mediated EMT and Invasion by Attenuation of IGF-1 Receptor Signaling in Breast Cancer. Journal of Cell Science 124(Pt 10):1752-1758, 2011. PMCID: PMC3085438.


Clark, J.L, Dresser, K., Chung-Cheng, H., Sabel, M.S., Kleer, C.G., Khan, A., and Shaw, L.M. Membrane Localization of Insulin Receptor Substrate-2 (IRS-2) Is Associated with Decreased Overall Survival in Breast Cancer. Breast Cancer Research and Treatment 130(3):759-772, 2011. PMCID: PMC3128655.


Kunju, L.P., Cookingham, C., Toy, K.A., Chen, W., Sabel, M.S, and Kleer, C.G. EZH2 and ALDH-1 Mark Breast Epithelium at Risk for Breast Cancer Development. Modern Pathology 24(6):786-93, 2011. PMCID: PMC3106137.


Liu, S., Ginestier, C., Ou, S.J., Clouthier, S.G., Patel, S.H., Monville, F., Korkaya, H., Heath, A., Dutcher, J., Kleer, C.G., Jung, Y., Dontu, G., Taichman, R., and Wicha, M.S. Breast Cancer Stem Cells Are Regulated by Mesenchymal Stem Cells through Cytokine Networks. Cancer Research 71(2):614-624, 2011. PMCID: PMC3100554.


Awuah, B., Martin, I.K., Takyi, V., Kleer, C.G., Nsiah-Asare, A., Aitpillah, F., and Newman, L. Implementation of a Percutaneous Core Needle Biopsy Training Program: Results from the University of Michigan-Komfo Anokye Teaching Hospital Breast Cancer Research Partnership. Annals of Surgical Oncology 18(4):957-960, 2011. PMCID: PMC3073403.


Toll, A.D., Dasgupta, A., Potoczek, M., Yeo, C.J., Kleer, C.G., Brody, J.R., and Witkiewicz, A.K. Implications of Enhancer of Zeste Homologue 2 Expression in Pancreatic Ductal Adenocarcinoma. Human Pathology 41(9):1205-1209, 2010. PMID: 20573371.


Stark, A., Kleer, C.G., Martin, I., Baffour, A., Asare, A.N., Takyi, V., Zarbo, R., Wicha, M.S., and Newman, L.A. African Ancestry and Higher Prevalence of Triple-negative Breast Cancer: Findings from an International Study. Cancer 116(21):4926-4932, 2010. PMCID: PMC3138711.


Huang, W., Gonzalez, M.E., Toy, K.A., Banerjee, M., and Kleer, C.G. Blockade of CCN6 (WISP3) Activates Growth Factor-independent Survival and Resistance to Anoikis in Human Mammary Epithelial Cells. Cancer Research 70(8):3340-3350, 2010. PMCID: PMC2856127.


Kleer, C.G. Pathology Re-review as an Essential Component of Breast Cancer Management. Current Oncology 17(1):2-3, 2010. PMCID: PMC2826772.


(2008 - 2009)          

Kleer, C.G. Carcinoma of the Breast with Medullary-like Features: Diagnostic Challenges and Relationship with BRCA1 and EZH2 Functions. Archives of Pathology & Laboratory Medicine 133(11):1822-1825, 2009. PMID: 19886718.


Lorenzatti G., Huang W., and Kleer C.G. The Emerging Role of CCN6 in Breast Cancer Invasion. Cell Science 6(2), 2009.


Pan, Q., Rosenthal, D.T., Bao, L., Kleer, C.G., and Merajver, S.D. Antiangiogenic Tetrathiomolybdate Protects Against Her2/neu-induced Breast Carcinoma by Hypoplastic Remodeling of the Mammary Gland.  Clinical Cancer Research 15(23):7441-7446, 2009. PMID: 19934283.


Li, X., Gonzalez, M.E., Toy, K., Filzen, T., Merajver, S.D., and Kleer, C.G. Targeted Overexpression of EZH2 in the Mammary Gland Disrupts Ductal Morphogenesis and Causes Epithelial Hyperplasia. The American Journal of Pathology 175(3):1246-1254, 2009. PMCID: PMC2731143.


Rhodes, D.R., Ateeq, B., Cao, Q., Tomlins, S.A., Mehra, R., Laxman, B., Kalyana-Sundaram, S., Lonigro, R.J., Helgeson, B.E., Bhojani, M.S., Rehemtulla, A., Kleer, C.G., Hayes, D.F., Lucas, P.C., Varambally, and S., Chinnaiyan, A.M. AGTR1 Overexpression Defines a Subset of Breast Cancer and Confers Sensitivity to Losartan, an AGTR1 Antagonist. Proceedings of the National Academy of Sciences of the United States of America 106(25):10284-10289, 2009. PMCID: PMC2689309.


Witkiewicz, A.K., Casimiro, M.C., Dasgupta, A., Mercier, I., Wang, C., Bonuccelli, G., Jasmin, J-F, Frank, P.G., Pestell, R.G., Kleer, C,G., Sotgia, F., and Lisanti, M.P. Towards a New “Stromal-based” Classification System for Human Breast Cancer Prognosis and Therapy. Cell Cycle 8(11):1654-1658, 2009. PMID: 19448435.


Witkiewicz, A.K., Dasgupta, A., Sotgia, F., Mercier, I., Pestell, R.G., Sabel, M., Kleer, C.G., Brody, J.R., and Lisanti, M.P. An Absence of Stromal Caveolin-1 Expression Predicts Early Tumor Recurrence and Poor Clinical Outcome in Human Breast Cancers. The American Journal of Pathology 174(6):2023-2034, 2009. PMCID: PMC2684168.


Sparano, J.A., Moulder, S., Kazi, A., Coppola, D., Negassa, A., Vahdat, L., Li, T., Pellegrino, C., Fineberg, S., Munster, P., Malafa, M., Lee, D., Hoschander, S., Hopkins, U., Hershman, D., Wright, J.J., Kleer, C.G., Merajver, S., and Sebti, S.M. Phase II trial of Tipifarnib Plus Neoadjuvant Doxorubicin-cyclophosphamide in Patients with Clinical Stage IIB-IIIC Breast Cancer. Clinical Cancer Research 15(8):2942-2948, 2009. PMCID: PMC2785076.


Lo, A-C, Georgopoulos, A., Kleer, C.G., Banerjee, M., Omar, S., Khaled, H., Eissa, S., Hablas, A., Omar, H.G., Douglas, J.A., Merajver, S.D., and Soliman, A.S. Analysis of RhoC Expression and Lymphovascular Emboli in Inflammatory Vs Non-inflammatory Breast Cancers in Egyptian Patients. Breast 18(1):55-59, 2009. PMCID: PMC2818070.


Lester, S.C., Bose, S., Chen, Y.Y., Connolly, J.L., de Baca, M.E., Fitzgibbons, P.L., Hayes, D.F., Kleer, C.G., O'Malley, F.P., Page, D.L., Smith, B.L., Weaver, D.L., and Winer, E. Protocol for Examination of Specimens from Patients with Ductal Carcinoma in Situ of the Breast. Archives of Pathology & Laboratory Medicine 133(1):15-25, 2009. PMID: 19123730.


Gonzalez, M.E., Li, X., Toy, K., DuPrie, M., Ventura, A.C., Banerjee, M., Ljungman, M., Merajver, S.D., and Kleer, C.G. Downregulation of EZH2 Decreases Growth of Estrogen Receptor-negative Invasive Breast Carcinoma and Requires BRCA1. Oncogene 28(6):843-853, 2009. PMCID: PMC2643353.


Sabel, M.S., Rogers, K., Griffith, K., Jagsi, R., Kleer, C.G., Diehl, K.A., Breslin, T.M., Cimmino, V.M., Chang, A.E., and Newman, L.A. Residual Disease After Re-excision Lumpectomy for Close Margins. Journal of Surgical Oncology 99(2):99-103, 2009. PMID: 19065638.


Cao, Q., Yu, J., Dhanasekaran, S.M., Kim, J.H., Mani, R-S, Tomlins, S.A., Mehra, R., Laxman, B., Cao, X.,  Yu, J., Kleer, C.G., Varambally, S., and Chinnaiyan, A.M. Repression of E-cadherin by the Polycomb Group Protein EZH2 in Cancer. Oncogene 27(58):7274-7284, 2008. PMCID: PMC2690514.


Kilbride, K.E., Lee, M.C., Nees, A.V., Cimmino, V.M., Diehl, K.I.M., Sabel, M.S., Hayes, D.F., Schott, A.F., Kleer, C.G., Chang, A.E., and Newman, L.A. Axillary Staging Prior to Neoadjuvant Chemotherapy for Breast Cancer: Predictors of Recurrence. Annals of Surgical Oncology 15(11):3252-3258, 2008. PMID: 18784961.


Kunju, L.P., Ding, Y., and Kleer, C.G. Tubular Carcinoma and Grade 1 (well-differentiated) Invasive Ductal Carcinoma: Comparison of Flat Epithelial Atypia and Other Intra-epithelial Lesions. Pathology International 58(10):620-625, 2008. PMID: 18801081.


Kleer, C.G.*, Bloushtain-Qimron, N.*, Chen, Y.-H., Carrasco, D., Hu, M., Yao, J., Kraeft, S, Collins, L.C., Sabel, M.S., Argani, P., Gelman, R., Schnitt, S.J., Krop, I.E., and Polyak, K. Epithelial and Stromal Cathepsin K and CXCL14 Expression in Breast Tumor Progression. Clinical Cancer Research 14(17):5357-5367, 2008. PMCID: PMC2630242.


Kunju, L., Ding, Y., and Kleer, C.G. Convergence Between Breast Flat Epithelial Atypia and Atypical Ductal Hyperplasia: Validity and Limitations. Human Pathology Sept 15, 2008.


Hayes, M.J., Thomas, D., Emmons (Witkiewicz), A., Giordano, T.J., and Kleer, C.G. Genetic Changes of Wnt Pathway Genes are Common Events in Metaplastic Carcinomas of the Breast. Clinical Cancer Research 14(13):4038-4044, 2008. PMCID: PMC3060761.


Huang, W., Zhang, Y., Varambally, S., Chinnaiyan, A.M., Banerjee, M., Merajver, S.D., and Kleer, C.G. Inhibition of CCN6 (Wnt-1-induced Signaling Protein 3) Down-regulates E-cadherin in the Breast Epithelium Through Induction of Snail and ZEB1. The American Journal of Pathology 172(4):893-904, 2008. PMCID: PMC2276413.


Liu, S., Ginestier, C., Charafe-Jauffret, E., Foco, H., Kleer, C.G., Merajver, S.D., Dontu, G., and Wicha, M.S. BRCA1 Regulates Human Mammary Stem/progenitor Cell Fate. Proceedings of the National Academy of Sciences of the United States of America 105(5):1680-1685, 2008. PMCID: PMC2234204.


Lo, A.C., Kleer, C.G.*, Banerjee, M., Omar, S., Khaled, H., Eissa, S., Hablas, A., Douglas, J.A., Alford, S.H., Merajver, S.D., and Soliman, A.S. Molecular Epidemiologic Features of Inflammatory Breast Cancer: a Comparison Between Egyptian and US Patients. Breast Cancer Research and Treament 112(1):141-147, 2008. PMCID: PMC3223859.

(2006 - 2007)

Ginestier, C.,  Hur, M.H., Charafe-Jauffret, E., Monville, F., Dutcher, J., Brown, M., Jacquemier, J., Viens, P.,  Kleer, C.G., Liu, S., Schott, A., Hayes, D.F., Birnbaum, D., Wicha, M.S., and Dontu, G. ALDH1 Is a Marker of Normal and Malignant Human Mammary Stem Cells and a Predictor of Poor Clinical Outcome. Cell Stem Cell 1(5):555-567, 2007. PMCID: PMC2423808.


Miao, Z., Luker, K.E., Summers, B.C., Berahovich, R., Bhojani, M.S., Rehemtulla, A., Kleer, C.G., Essner, J.J., Nasevicius, A., Luker, G.D., Howard, M.C., and Schall, T.J. CXCR7 (RDC1) Promotes Breast and Lung Tumor Growth in Vivo and is Expressed on Tumor-associated Vasculature. Proceedings of the National Academy of Sciences of the United States of America 104(40):15735-15740, 2007. PMCID: PMC1994579.


Zakaria, S., Degnim, A.C., Kleer, C.G., Diehl, K.A., Cimmino, V.M., Chang, A.E., Newman, L.A., and Sabel, M.S. Sentinel Lymph Node Biopsy for Breast Cancer: How Many Nodes Are Enough? Journal of Surgical Oncology 96(7):554-559, 2007. PMID: 17685432.


Glaros, S., Cirrincione, G.M., Muchardt, C., Kleer, C.G., Michael, C.W., and Reisman, D. The Reversible Epigenetic Silencing of BRM: Implications for Clinical Targeted Therapy. Oncogene 26(49):7058-7066, 2007. PMID: 17546055.


McHugh, J.B., Fullen, D.R., Ma, L., Kleer, C.G., and Su, L.D. Expression of Polycomb Group Protein EZH2 in Nevi and Melanoma. Journal of Cutaneous Pathology 34(8):597-600, 2007. PMID: 17640228.


Privette, L.M., González, M.E., Ding, L., Kleer, C.G., and Petty E.M. Altered Expression of the Early Mitotic Checkpoint Protein, CHFR, in Breast Cancers: Implications for Tumor Suppression. Cancer Research 67(13):6064-6074, 2007. PMID: 17596595.


Kleer, C.G., Zhang, Y, and Merajver, SD. CCN6 (WISP3) as a New Regulator of the Epithelial Phenotype in Breast Cancer. Cells, Tissues, Organs 185(1-3):95-99, 2007. PMID: 17587813.


Newman, E.A., Sabel, M.S., Nees, A.V., Schott, A., Diehl, K.M. Cimmino, V.M., Chang, A.E., Kleer, C.G., Hayes, D.F., and Newman, L.A. Sentinel Lymph Node Biopsy Performed After Neoadjuvant Chemotherapy is Accurate in Patients with Documented Node-positive Breast Cancer at Presentation. Annals of Surgical Oncology 14(10):2946-2952, 2007. PMID: 17514407.


Ostrander, J.H., Daniel, A.R., Lofgren, K., Kleer, C.G., and Lange, C.A. Breast Tumor Kinase (protein Tyrosine Kinase 6) Regulates Heregulin-induced Activation of ERK5 and P38 MAP Kinases in Breast Cancer Cells. Cancer Research 67(9):4199-4209, 2007. PMID: 17483331.


Kunju, L.P. and Kleer, C.G. Significance of Flat Epithelial Atypia on Mammotome Core Needle Biopsy: Should it be Excised? Human Pathology 38(1):35-41, 2007. PMID: 17095059.


Zeidler, M. and Kleer, C.G. The Polycomb Group Protein Enhancer of Zeste 2: Its Links to DNA Repair and Breast Cancer. Journal of Molecular Histology 37(5-7):219-223, 2006. PMID: 16855786.


Ding, L. and Kleer, C.G. Enhancer of Zeste 2 as a Marker of Preneoplastic Progression in the Breast. Cancer Research 66(19):9352-9355, 2006. PMID: 17018586.


Kleer, C.G., Teknos, T.N., Islam, M., Marcus, B., Lee, J.S.J., Pan, Q., and Merajver, S.D.  RhoC-GTPase Expression as a Potential Marker of Lymph Node Metastasis in Squamous Cell Carcinomas of the Head and Neck. Clinical Cancer Research 12(15):4485-4490, 2006. PMID: 16899593.


Newman, E.A., Guest, A.B., Helvie, M.A., Roubidoux, M.A., Chang, A.E., Kleer, C.G., Diehl, K.M., Cimmino, V.M., Pierce, L.J., Hayes, D., Newman, L.A., and Sabel, M.S. Changes in Surgical Management Resulting from Case Review at a Breast Cancer Multidisciplinary Tumor Board. Cancer 107(10):2346-2351, 2006. PMID: 16998942.


Kuefer, R., Day, K.C., Kleer, C.G., Sabel, M.S., Hofer, M.D., Varambally, S., Zorn, C.S., Chinnaiyan, A.M., Rubin, M.A., and Day, M.L. The ADAM15 Disintegrin is Associated with Aggressive Prostate and Breast Cancer Disease. Neoplasia 8(4): 319-329, 2006. PMCID: PMC1600681.


Hird, R.B., Chang, A., Cimmino, V., Diehl, K., Sabel, M., Kleer, C.G., Helvie, M., Schott, A., Young, J., Hayes, D., and Newman, L. Impact of Estrogen Receptor Expression and Other Clinicopathologic Features on Tamoxifen Use in Ductal Carcinoma in Situ. Cancer 106(10):2113-2118, 2006. PMID: 16596655.


Ding, L., Erdmann, C., Chinnaiyan, A.M., Merajver, S.D., and Kleer, C.G. Identification of EZH2 as a Molecular Marker for a Precancerous State in Morphologically Normal Breast Tissues. Cancer Research 66(8):4095-4099, 2006. Selected as a Cancer Research Highlight. PMID: 16618729.


Newman, E.L., Kahn, A., Diehl, K.M., Cimmino, V.M., Kleer, C.G., Chang, A.E., Newman, L.A., and Sabel, M.S. Does the Method of Biopsy Affect the Incidence of Sentinel Lymph Node Metastases? The Breast Journal 12(1):53-57, 2006. PMID: 16409587.


O’Malley, F.P., Mohsin, S.K., Badve, S., Bose, S., Collins, L.C., Ennis, M., Kleer, C.G., Pinder, S.E., and Schnitt, S.J. Interobserver Reproducibility in the Diagnosis of Flat Epithelial Atypia of the Breast. Modern Pathology 19(2):172-179, 2006. PMID: 16424892.


Ben-David, M.A., Kleer, C.G., Paramagul, C., Griffith, K.A., and Pierce, L.J. Is Lobular Carcinoma in Situ as a Component of Breast Carcinoma a Risk Factor for Local Failure After Breast-conserving Therapy? Results of a Matched Pair Analysis. Cancer 106(1):28-34, 2006. PMID: 16329136.

(2004 - 2005)

Paramagul, C.P., Helvie, M.A., Robidoux, M.A., Kleer, C.G., and Newman, L.A. Lobular Carcinoma in Situ (LCIS): Clinical and Mammography Findings of Subsequent Breast Cancers. Journal of Women’s Imaging 7(4):181-189, 2005.


Krop, I., März, A., Carlsson, H., Li, X., Bloushtain-Qimron, N., Hu, M., Gelman, R., Sabel, M.S., Schnitt, S., Ramaswamy, S., Kleer, C.G., Enerbäck, C., and Polyak, K. A Putative Role for Psoriasin in Breast Tumor Progression. Cancer Research 65(24):11326-11334, 2005. PMID: 16357139.


Mehra, R., Varambally, S., Shen, R., Ding, L., Shen, R., Sabel, M.S., Ghosh, D., Chinnaiyan, A.M.*, and Kleer, C.G.* Identification of GATA3 as a Breast Cancer Prognostic Marker by Global Gene Expression Meta-analysis. Cancer Research 65(24):11259-11264, 2005. PMID: 16357129.


Zhang, Y., Pan, Q., Zhong, H., Merajver, S.D., and Kleer, C.G. Inhibition of CCN6 (WISP3) Expression Promotes Neoplastic Progression and Enhances the Effects of Insulin-like Growth Factor-1 on Breast Epithelial Cells. Breast Cancer Research 7(6):R1080-1089, 2005. PMCID: PMC1410771.


Zeidler, M., Varambally, S., Cao, Q., Chinnaiyan, A.M., Ferguson, D.O., Merajver, S.D., and Kleer, C.G. The Polycomb Group Protein EZH2 Impairs DNA Repair in Breast Epithelial Cells. Neoplasia 7(11):1011-1019, 2005. Featured article and Cover. PMCID: PMC1502020.


Pan, Q., Bao, L.W., Kleer, C.G., Sabel, M., and Merajver, S.D. Protein Kinase C Epsilon is a Predictive Biomarker of Aggressive Breast Cancer and a Validated Target for RNA Interference Anticancer Therapy. Cancer Research 65(18):8366-8371, 2005. PMID: 16166314.


Kleer, C.G., Griffith, K., Sabel, M.S., van Golen, K.L., Gallagher, G., Wu, Z-F, and Merajver, S.D. RhoC-GTPase is a Novel Tissue Biomarker Associated with Biologically Aggressive Carcinomas of the Breast. Breast Cancer Research and Treatment 93(2):101-110, 2005. PMID: 16187229.


Schott, A.F., Roubidoux, M.A., Helvie, M.A., Hayes, D.F., Kleer, C.G., Newman, L.A., Pierce, L.J., Griffith, K.A., Murray, S., Hunt, K.A., Paramagul, C., and Baker, L.H. Clinical and Radiologic Assessments to Predict Breast Cancer Pathologic Complete Response to Neoadjuvant Chemotherapy. Breast Cancer Research and Treatment 92(3):231-238, 2005. PMID: 16155794.


Khan, A., Sabel, M.S., Nees, A., Diehl, K.M., Cimmino, V.M., Kleer, C.G., Schott, A.F., Hayes, D.F., Chang, A.E., and Newman, L.A. Comprehensive Axillary Evaluation in Neoadjuvant Chemotherapy Patients with Ultrasonography and Sentinel Lymph Node Biopsy. Annuals of Surgical Oncology 12(9):697-704, 2005. PMID: 16079956.


Witkiewicz, A.K, Varambally, S., Shen, R., Mehra, R., Chinnaiyan, A.M., Sabel, M.S., Ghosh, D., Chinnaiyan, A.M., Rubin, M.A., and Kleer, C.G.  Alpha-methylacyl-CoA Racemase Protein Expression is Associated with the Degree of Differentiation in Breast Cancer Using Quantitative Image Analysis. Cancer Epidemiology, Biomarkers & Prevention 14(6):1418-1423, 2005. PMID: 15941950.


Pu, R.T., Schott, A.F., Sturtz, D.E., Griffith, K.A., and Kleer, C.G. Pathologic Features of Breast Cancer Associated with Complete Response to Neoadjuvant Chemotherapy: Importance of Tumor Necrosis. The American Journal of Surgical Pathology 29(3):354-58, 2005. PMID: 15725804.


Stearns, V., Gallagher, A., Kleer, C.G., Singh, B., Freedman, M., Haddad, B., Isaacs, C., Warren, R., Brown, M., Trock, B., and Hayes, D.F. A Pilot Study to Establish a Clinical Model to Perform Phase II Studies of Breast Cancer Chemopreventive Agents in Women at High Risk Using Biomarkers as Surrogate Endpoints for Activity. Clinical Cancer Research 10(24):8332-8340, 2004. PMID: 15623610.


Kleer, C.G., Zhang, Y., Pan, Q., Gallagher, G., Wu, M., Wu, Z-F, and Merajver, S.D. WISP3 and RhoC Guanosine Triphosphatase Cooperate in the Development of Inflammatory Breast Cancer. Breast Cancer Research 6(2):R110-115, 2004. PMID: 15602803.


Roubidoux, M.A., Sabel, M.S., Bailey, J.E., Kleer, C.G., Klein, K.A., and Helvie, M.A. Small (<2.0-cm) Breast Cancers: Mammographic and US Findings at US-guided Cryoablation--initial Experience. Radiology 233(3):857-867, 2004. PMID: 15567802.


Marcus, B., Arenberg, D., Lee, J., Kleer, C.G., Chepeha, D.B., Schmalbach, C.E., Islam, M., Pan, Q., Hanash, S., Kuick, R., Merajver, S.D., and Teknos, T.N. Prognostic Factors in Oral Cavity and Oropharyngeal Squamous Cell Carcinoma. Cancer 101(12):2779-2787, 2004. PMID: 15546137.


Koker, M.M. and Kleer, C.G. P63 Expression in Breast Cancer: a Highly Sensitive and Specific Marker of Metaplastic Carcinoma. The American Journal of Surgical Pathology 28(11):1506-1512, 2004. PMID: 15489655.


Kleer, C.G., Zhang, Y., Pan, Q., and Merajver, S.D. WISP3 (CCN6) Is a Secreted Tumor-suppressor Protein That Modulates IGF Signaling in Inflammatory Breast Cancer. Neoplasia 6(2):179-185, 2004. PMCID: PMC1502087.


Van den Eynden, G.G., Van der Auwera, I., Van Laere, S., Colpaert, C.G., van Dam, P., Merajver, S.D., Kleer, C.G., Harris, A.L., Van Marck, E.A., Dirix, L.Y., and Vermeulen, P.B. Validation of a Tissue Microarray to Study Differential Protein Expression in Inflammatory and Non-Inflammatory Breast Cancer. Breast Cancer Research and Treatment 85(1):13-22, 2004. PMID: 15039594.


Ray, M.E., Yang, Z.Q., Albertson, D., Kleer, C.G., Washburn, J.G., Macoska, J.A., and Ethier, S.P. Genomic and Expression Analysis of the 8p11-12 Amplicon in Human Breast Cancer Cell Lines. Cancer Research 64(1):40-47, 2004. PMID: 14729606.

(1996 - 2003)

Kowalski, P.J., Rubin, M.A., and Kleer, C.G. E-cadherin Expression in Primary Carcinomas of the Breast and Its Distant Metastases. Breast Cancer Research 5(6):R217-222, 2003. PMCID: PMC314411.


Kleer, C.G.*, Cao, Q.*, Varambally, S.*, Shen, R., Ota, I., Tomlins, S.A., Ghosh, D., Sewalt, R.G., Otte, A.P., Hayes, D.F., Sabel, M.S., Livant, D., Weiss, S.J., Rubin, M.A., and Chinnaiyan, A.M. EZH2 Is a Marker of Aggressive Breast Cancer and Promotes Neoplastic Transformation of Breast Epithelial Cells. Proceedings of the National Academy of Sciences 100(20):11606-11611, 2003. PMCID: PMC208805.


Collisson, E.A., Kleer, C.G., Wu, M., De, A., Gambhir, S.S., Merajver, S.D., and Kolodney, M.S. Atorvastatin Prevents RhoC Isoprenylation, Invasion, and Metastasis in Human Melanoma Cells. Molecular Cancer Therapeutics 2(10):941-948, 2003. PMID: 14578459.


Pan, Q., Bao, L.W., Kleer, C.G., Brewer, G.J., and Merajver, S.D. Antiangiogenic Tetrathiomolybdate Enhances the Efficacy of Doxorubicin Against Breast Carcinoma. Molecular Cancer Therapeutics 2(7):617-622, 2003. PMID: 12883034.


Sabel, M.S., Schott, A.F., Kleer, C.G., Merajver, S.D., Cimmino, V.M., Diehl, K.M., Hayes, D.F., Chang, A.E., and Pierce, L.J. Sentinel Node Biopsy Prior to Neoadjuvant Chemotherapy. American Journal of Surgery 186(2):102-105, 2003. PMID: 12885598.


Rao, D.S., Bradley, S.V., Kumar, P.D., Hyun, T.S., Saint-Dic, D., Oravecz-Wilson, K., Kleer, C.G., and Ross, T.S. Altered Receptor Trafficking in Huntingtin Interacting Protein 1-transformed Cells. Cancer Cell 3(5):471-482, 2003. PMID: 12781365.


Valdez, R., Thorson, J., Finn, W.G., Schnitzer, B., and Kleer, C.G. Lymphocytic Mastitis and Diabetic Mastopathy: a Molecular, Immunophenotypic, and Clinicopathologic Evaluation of 11 Cases. Modern Pathology 16(3):223-228, 2003. PMID: 12640102.


Zhou, M., Chinnaiyan, A.M., Kleer, C.G., Lucas, P.C., and Rubin, M.A. Alpha-Methylacyl-CoA Racemase: a Novel Tumor Marker Over-expressed in Several Human Cancers and Their Precursor Lesions. The American Journal of Surgical Pathology 26(7):926-931, 2002. PMID: 12131161.


Pan, Q., Kleer, C.G., van Golen, K.L., Irani, J., Bottema, K.M., Bais, C., De Carvalho, M., Mesri, E.A., Robins, D.M., Dick, R., Brewer, G.J., and Merajver, S.D. Copper Deficiency Induced by Tetrathiomolybdate Suppresses Tumor Growth and Angiogenesis. Cancer Research 62(17):4854-4859, 2002. PMID: 12208730.


Kleer, C.G., Zhang, Y., Pan, Q., van Golen, K.L., Wu, Z-F, Livant, D., and Merajver, S.D. WISP3 Is a Novel Tumor Suppressor Gene of Inflammatory Breast Cancer. Oncogene 21(20):3172-3180, 2002. PMID: 12082632.


Kleer, C.G., van Golen, K.L., Zhang, Y., Wu, Z-F, Rubin, M.A., and Merajver, S.D. Characterization of RhoC Expression in Benign and Malignant Breast Disease: a Potential New Marker for Small Breast Carcinomas with Metastatic Ability. The American Journal of Pathology 160(2):579-584, 2002. PMCID: PMC1850656.


Kleer, C.G., Tseng, M.D., Gutsch, D.E., Rochford, A.R., Wu, Z-F, Joynt, L.K., Helvie, M.A., Chang, T., van Golen, K.L., and Merajver, S.D. Epstein-Barr Virus is Implicated in the Pathogenesis of Breast Fibroadenomas in Immunocompromised Hosts. Modern Pathology 15(7):759-764, 2002.


Kleer, C.G. and Merajver, S.D. The Pathology of Familial Breast Cancer: Predictive Value of Estrogen Receptor, Progesterone Receptor, HER-2, and P53 in Patients with Mutations in BRCA1 and BRCA2. The American Journal of Oncology Review 1(4):194-195, 2002.


Kleer, C.G., van Golen, K.L., Braun, T., and Merajver, S.D. Persistent E-cadherin Expression in Inflammatory Breast Cancer. Modern Pathology 14(5):458-464, 2001. PMID: 11353057.


Kleer, C.G., Giordano, T.G., Braun, T., and Oberman, H.A. Pathologic, Immunohistochemical, and Molecular Features of Benign and Malignant Phyllodes Tumors of the Breast. Modern Pathology 14(3):185-190, 2001. PMID: 11266524.


Kleer, C.G., van Golen, K.L., and Merajver, S.D. Molecular Biology of Breast Cancer Metastasis. Inflammatory Breast Cancer: Clinical Syndrome and Molecular Determinants. Breast Cancer Research 2(6):423-429, 2000. PMCID: PMC138665.


Kleer, C.G. and Michael, C.W. Fine-needle Aspiration of Breast Carcinomas with Prominent Lymphocytic Infiltrate. Diagnostic Cytopathology 23(1):39-42, 2000. PMID: 10907931.


Kleer, C.G, Giordano, T.J., and Merino, M.J. Squamous Cell Carcinoma of the Thyroid: An Aggressive Tumor Associated with Tall Cell Variant of Papillary Thyroid Carcinoma. Modern Pathology 13(7):742-746, 2000. PMID: 10912933.


Kleer, C.G., Bryant, B.R., Giordano, T.J., Sobel, M.E., and Merino, M.J. Genetic Changes in Chromosomes 1p and 17p in Thyroid Cancer Progression. Endocrine Pathology 11(2):137-143, 2000. PMID: 12114819.


Kim, B., Barnett, J.L., Kleer, C.G., and Appelman, H.D. Endoscopic and Histological Patchiness in Treated Ulcerative Colitis. The American Journal of Gastroenterology 94(11):3258-3262, 1999. PMID: 10566726.


Kleer, C.G., Wojno, K.J., Fields, K., and Singleton, T.P. Detection of Estrogen Receptor in Carcinomas of the Breast Using Automated Immunohistochemistry. Journal of Applied Immunohistochemistry and Molecular Morphology 7(2):103-107, 1999.


Carlson, K.L., Helvie, M.A., Roubidoux, M.A., Kleer, C.G., Oberman, H.A., Wilson T.E., Pollak, E.W., and Rochester, A.B. Relationship Between Mammographic Screening Intervals and Size and Histology of Ductal Carcinoma in Situ. American Journal Roentgenology 172(2):313-317, 1999. PMID: 9930774.


Kleer, C.G. and Oberman, H.A. Adenoid Cystic Carcinoma of the Breast: Value of Histologic Grading and Proliferative Activity. The American Journal of Surgical Pathology 22(5):569-575, 1998. PMID: 9591727.


Kleer, C.G. and Appelman, H.D. Ulcerative Colitis: Patterns of Involvement in Colorectal Biopsies and Changes with Time. The American Journal of Surgical Pathology 22(8):983-989, 1998. PMID: 9706978.


Goh, M., Kleer, C.G., Kielczewski, P., Wojno, K.J., Kim, K., and Oesterling, J.E. Autologous Blood Donation Prior to Anatomical Radical Retropubic Prostatectomy: Is It Necessary? Urology 49(4):569-573, 1997. PMID: 9111627.


Kleer, C.G., Unni, K.K., and McLeod, R.A. Epithelioid Hemangioendothelioma of Bone. The American Journal of Surgical Pathology 20(11):1301-1311, 1996.

Book Chapters

  1. Feldstein, C.G. (Kleer), Romero, J.C., Ruilope, L., Lahera, V. Humoral Regulation of Glomerular Hemodynamics in Hypertension.  Molecular Cell Biology of Cardiovascular Diseases 86-95. Mosby/Doyma, Libros, Madrid, Spain, 1995.
  1. Kleer, C.G. and Appelman, H.D. Surgical Pathology of Crohn’s Disease. Surgical Clinics of North America 81(1):13-30, Vii, Feb 2001.
  1. Kleer, C.G., Ding, L. WISP3 (WNT-1 inducible Signaling Pathway Protein 3). Atlas Genet Cytogenetic Oncology Hematology, Mar 2005.
  1. Kleer, C.G. Polycomb Group Proteins. Encyclopedia of Cancer, Second Edition 2007. Editor: Manfred Schwab. Springer-Verlag, Germany.
  1. Maturen, K.E., Paramagul, C.P., Roubidoux, M.A., Kleer, C.G., Weadock W.J., Abate, S.A.  Interactive Computer Teaching Module for Radiologic-Pathologic Correlations in Breast Imaging. MedEdPORTAL, http://www.med.umich.edu/rad/b-imaging/edu/MammoWEB.swf
  1. Kleer, C.G. CCN6 (WISP3) as a Regulator of EMT: Implications in Breast Cancer Metastasis. Human Epithelial Tumor Cell Plasticity: Implications for Cancer Progression and Metastasis 59-68.Editor: Paul J. Higgins. Research Signpost, India, 2008.
  1. Pal A, Huang W, Kleer, C.G. CCN6 as a Modulator of Growth Factor Signaling Pathways: Implications for Breast Cancer Growth and Invasion. Proceedings of the CCN Society, 2009.
  1. Kleer, C.G., and Sabel M.S. Prognostic and Predictive Factors in Breast Cancer. In Kuerer’s Breast Surgical Oncology, 2nd Edition (editor, Henry Kuerer, MD, PhD, FACS) McGraw-Hill Professional, New York, 2010.