Suranganie Dharmawardhane
Title | PhD |
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Faculty Rank | Associate Professor |
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Institution | University of Puerto Rico |
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Department | School of Medicine |
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Address | UPR-Medical Sciences Campus, School of Medicine San Juan PR 936
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Phone | 7877582525 ext. 1630 |
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vCard | Download vCard |
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Title | Adjunct Associate Professor |
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Institution | Universidad Central Del Caribe |
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Department | Biochemistry |
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Biography
1999 - 2003 | Scientist Development Award, American Heart Association, National |
Overview
I have spent the past 13 years directing a viable program in breast cancer metastasis and the preventive and therapeutic role of natural and synthetic anti-metastasis compounds. My postdoctoral training was from Dr. John Condeelis (Albert Einstein College of Medicine, NY), who is a pioneering authority on in vivo image analysis of breast cancer metastasis. I was subsequently trained in molecular biology and analysis of cell signaling of model systems (Dictyostelium) and fibrobalsts and leukocytes in the laboratories of Dr. Richard Firtel (University of California, San Diego) and Dr. Gary Bokoch (Scripps Research Institute, CA). During my Assistant Professorship at the University of Texas at Austin (1999-2005), in collaboration with biomedical engineers, we designed and developed methodology for whole body and microscopic fluorescence image analysis of fluorescently-tagged breast cancer cells in mouse models. This technology and my research program in breast cancer metastasis have been transferred to my current research group at the University of Puerto Rico Medical Sciences Campus (UPR MSC), San Juan, PR.
At UPR MSC, we have continued with investigation of the effects and molecular mechanisms of red wine and soy polyphenols using human breast cancer cell lines and immunocompromised mouse models. In collaboration with medicinal chemists (Drs. Eliud Hernandez and Cornelis Vlaar, School of Pharmacy), we are designing and characterizing novel small molecule inhibitors to the small GTPase Rac, a central regulator of motility in normal and cancer cells. We have a pending patent for the small molecule EHop-016 that we are developing as an anti metastatic breast cancer therapeutic. Our recent collaborations with Dr. George Calin (MD Anderson Cancer Center, Houston, TX), has led to an investigation on the role of non-coding RNA (ncRNA) in breast cancer therapy resistance. We have also initiated a collaborative study with Dr. Naima Moustaid-Moussa (Texas Tech University) to investigate molecular mechanisms and targeted therapeutics for obesity-associated breast cancer metastasis in postmenopausal women.
My commitment to cancer research is reflected in 39 pubmed citations, of which 18 (2002-2012) are from my independent research program in breast cancer. I am an active member of the American Society of Cell Biologists (ASCB), American Association for Cancer Research (AACR), and the American Society for Biochemistry and Molecular Biology (ASBMB). I have also served as a review panel member of the US Army Department of Defense (DoD)/Ovarian Cancer Research and Breast Cancer Research Programs (BCRP) and acted as an ad-hoc reviewer for the NIH Basic Mechanisms of Cancer Therapeutics study section. My research has received funding from NIH/NCI, DoD/BCRP and the American Institute of Cancer Research. I was also the recipient of a Cancer Research Center Grant (role: Director) that I submitted with the RCMI Program of Universidad Central del Caribe (UCC), 5G12RR003035, that was relinquished after my move to UPR MSC.
I also enjoy and have had successful experiences with mentoring undergraduate, graduate, medical, and post-doctoral students, as well as Assistant Professors. Most of my undergraduate mentees have gone on to Ph.D and M.D. Programs. I graduated two M.Sc. students and 5 Ph.D. students who went on to postdoctoral positions in prestigious institutions. My first graduate student Dr. Paige Baugher is a tenured Associate Professor with her own breast cancer research program at Pacific University, Oregon. I have trained eight postdoctoral (6 Ph.D.s and 2 M.D.s) researchers who are currently in academia or medical residencies. During my tenure at UCC (Bayamon, PR) as chief of the Cell Biology section, I mentored two assistant professors: Dr. Valance Washington was the successful recipient of a MBRS/SC2, who then went on to receive a R01 award. Dr. Michelle Martínez currently holds three pilot project awards from NIH grants to UCC and UPR. My current mentee from the UPRCCC, Dr. Pablo Vivas was recently awarded a NIH/NCI/K22 grant. I am currently training four Ph.D. students and an Assistant Professor in my research group. Therefore, my extensive training record exemplifies my commitment to mentoring women and minorities to become productive biomedical researchers and academics.
Research
R21CA083957 (DHARMAWARDHANE, SURANGANIE F)May 1, 2000 - Apr 30, 2003 NIH REGULATORY ROLE OF RAC AND CDC42 ON TUMOR METASTASIS Role: Principal Investigator |
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R03CA109913 (DHARMAWARDHANE, SURANGANIE F)Apr 1, 2005 - Mar 31, 2007 NIH Resveratrol in breast cancer cell survival or apoptosis Role: Principal Investigator |
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SC3GM084824 (DHARMAWARDHANE, SURANGANIE F)Sep 10, 2008 - Jun 30, 2022 NIH Targeting breast cancer progression Role: Principal Investigator |
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R16GM149427 (DHARMAWARDHANE, SURANGANIE)May 2, 2023 - Apr 30, 2027 NIH MBQ-167 derivatives as antimetastatic cancer agents. Role: Principal Investigator |
Bibliographic
PMC Citations indicate the number of times the publication was cited by articles in PubMed Central, and the Altmetric score represents citations in news articles and social media.
(Note that publications are often cited in additional ways that are not shown here.)
Fields are based on how the National Library of Medicine (NLM) classifies the publication's journal and might not represent the specific topic of the publication.
Translation tags are based on the publication type and the MeSH terms NLM assigns to the publication.
Some publications (especially newer ones and publications not in PubMed) might not yet be assigned Field or Translation tags.)
Click a Field or Translation tag to filter the publications.
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Cruz-Collazo AM, Katsara O, Grafals-Ruiz N, Colon Gonzalez J, Dorta-Estremera S, Carlo VP, Chorna N, Schneider RJ, Dharmawardhane S. Novel inhibition of central carbon metabolism pathways by Rac and Cdc42 inhibitor MBQ-167 and paclitaxel. Mol Cancer Ther. 2024 Aug 01.
PMID: 39087451.
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Vel?zquez-Vega LE, Rivera-Robles M, S?nchez-?lvarez AO, Vivas-Mej?a PE, Aponte-Reyes M, Cruz-Collazo AM, Grafals-Ruiz N, Dorta-Estremera S, Hern?ndez-O'Farrill E, Vlaar CP, Dharmawardhane S. Efficacy and delivery strategies of the dual Rac/Cdc42 inhibitor MBQ-167 in HER2 overexpressing breast cancer. Transl Oncol. 2024 Jun; 44:101928.
PMID: 38489873.
Citations:
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Alsina-S?nchez ?M, Montalvo-V?zquez S, Grafals-Ruiz N, Acosta C, Orm? EM, Rodr?guez I, Delgado-Rivera SM, Tinoco AD, Dharmawardhane S, Montes-Gonz?lez IC. Synthesis of Novel Heterocyclic Ferrocenyl Chalcones and Their Biological Evaluation. ACS Omega. 2023 Sep 26; 8(38):34377-34387.
PMID: 37779926.
Citations:
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Torres-Sanchez A, Rivera-Robles M, Castillo-Pichardo L, Mart?nez-Ferrer M, Dorta-Estremera SM, Dharmawardhane S. Rac and Cdc42 inhibitors reduce macrophage function in breast cancer preclinical models. Front Oncol. 2023; 13:1152458.
PMID: 37397366.
Citations:
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Medina JI, Cruz-Collazo A, Del Mar Maldonado M, Gascot TM, Borrero-Garcia LD, Cooke M, Kazanietz MG, O'Farril EH, Vlaar CP, Dharmawardhane S. Characterization of Novel Derivatives of MBQ-167, an inhibitor of the GTP-binding proteins Rac/Cdc42. Cancer Res Commun. 2022 12; 2(12):1711-1726.
PMID: 36861094.
Citations:
3 Fields:
Translation:
Animals
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Cruz-Collazo A, Ruiz-Calderon JF, Picon H, Borrero-Garcia LD, Lopez I, Castillo-Pichardo L, Del Mar Maldonado M, Duconge J, Medina JI, Bayro MJ, Hern?ndez-O'Farrill E, Vlaar CP, Dharmawardhane S. Efficacy of Rac and Cdc42 Inhibitor MBQ-167 in Triple-negative Breast Cancer. Mol Cancer Ther. 2021 12; 20(12):2420-2432.
PMID: 34607932.
Citations:
7 Fields:
Translation:
HumansAnimalsCells
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Lacourt-Ventura MY, Vilanova-Cuevas B, Rivera-Rodr?guez D, Rosario-Acevedo R, Miranda C, Maldonado-Mart?nez G, Maysonet J, Vargas D, Ruiz Y, Hunter-Mellado R, Cubano LA, Dharmawardhane S, Lampe JW, Baerga-Ortiz A, Godoy-Vitorino F, Mart?nez-Montemayor MM. Soy and Frequent Dairy Consumption with Subsequent Equol Production Reveals Decreased Gut Health in a Cohort of Healthy Puerto Rican Women. Int J Environ Res Public Health. 2021 08 04; 18(16).
PMID: 34444002.
Citations:
2 Fields:
Translation:
Humans
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Borrero-Garc?a LD, Del Mar Maldonado M, Medina-Vel?zquez J, Troche-Torres AL, Velazquez L, Grafals-Ruiz N, Dharmawardhane S. Rac inhibition as a novel therapeutic strategy for EGFR/HER2 targeted therapy resistant breast cancer. BMC Cancer. 2021 Jun 01; 21(1):652.
PMID: 34074257.
Citations:
7 Fields:
Translation:
HumansCells
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Dharmawardhane S. Rho Family GTPases in Cancer. Cancers (Basel). 2021 Mar 12; 13(6).
PMID: 33809395.
Citations:
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Reig-L?pez J, Maldonado MDM, Merino-Sanjuan M, Cruz-Collazo AM, Ruiz-Calder?n JF, Mangas-Sanju?n V, Dharmawardhane S, Duconge J. Physiologically-Based Pharmacokinetic/Pharmacodynamic Model of MBQ-167 to Predict Tumor Growth Inhibition in Mice. Pharmaceutics. 2020 Oct 15; 12(10).
PMID: 33076517.
Citations:
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Maldonado MDM, Medina JI, Velazquez L, Dharmawardhane S. Targeting Rac and Cdc42 GEFs in Metastatic Cancer. Front Cell Dev Biol. 2020; 8:201.
PMID: 32322580.
Citations:
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Mendez B, Reyes J, Conde I, Ramos Z, Lozada E, Cruz AM, Asencio G, Carvajal A, Dharmawardhane S, Pi?ero-Cruz DM, Hern?ndez E, Vivas P, Ospina CA. Simalikalactone D, a Potential Anticancer Compound from Simarouba tulae, an Endemic Plant of Puerto Rico. Plants (Basel). 2020 Jan 11; 9(1).
PMID: 31940804.
Citations:
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Maldonado MDM, Rosado-Gonz?lez G, Bloom J, Duconge J, Ruiz-Calder?n JF, Hern?ndez-O'Farrill E, Vlaar C, Rodr?guez-Orengo JF, Dharmawardhane S. Pharmacokinetics of the Rac/Cdc42 Inhibitor MBQ-167 in Mice by Supercritical Fluid Chromatography-Tandem Mass Spectrometry. ACS Omega. 2019 Nov 05; 4(19):17981-17989.
PMID: 31720502.
Citations:
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Al-Jawadi A, Rasha F, Ramalingam L, Alhaj S, Moussa H, Gollahon L, Dharmawardhane S, Moustaid-Moussa N. Protective effects of eicosapentaenoic acid in adipocyte-breast cancer cell cross talk. J Nutr Biochem. 2020 01; 75:108244.
PMID: 31704550.
Citations:
8 Fields:
Translation:
HumansAnimalsCells
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Butler-Fern?ndez KM, Ramos Z, Francis-Malav? AM, Bloom J, Dharmawardhane S, Hern?ndez E. Synthesis, Anti-Cancer and Anti-Migratory Evaluation of 3,6-Dibromocarbazole and 5-Bromoindole Derivatives. Molecules. 2019 Jul 24; 24(15).
PMID: 31344865.
Citations:
2 Fields:
Translation:
HumansCells
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Rivera-Robles MJ, Medina-Vel?zquez J, Asencio-Torres GM, Gonz?lez-Crespo S, Rymond BC, Rodr?guez-Medina J, Dharmawardhane S. Targeting Cdc42 with the anticancer compound MBQ-167 inhibits cell polarity and growth in the budding yeast S. cerevisiae. Small GTPases. 2020 11; 11(6):430-440.
PMID: 29969362.
Citations:
6 Fields:
Translation:
AnimalsCells
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Maldonado MDM, Dharmawardhane S. Targeting Rac and Cdc42 GTPases in Cancer. Cancer Res. 2018 06 15; 78(12):3101-3111.
PMID: 29858187.
Citations:
136 Fields:
Translation:
HumansCells
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Al-Jawadi A, Moussa H, Ramalingam L, Dharmawardhane S, Gollahon L, Gunaratne P, Layeequr Rahman R, Moustaid-Moussa N. Protective properties of n-3 fatty acids and implications in obesity-associated breast cancer. J Nutr Biochem. 2018 03; 53:1-8.
PMID: 29096149.
Citations:
14 Fields:
Translation:
HumansAnimals
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Humphries-Bickley T, Castillo-Pichardo L, Hernandez-O'Farrill E, Borrero-Garcia LD, Forestier-Roman I, Gerena Y, Blanco M, Rivera-Robles MJ, Rodriguez-Medina JR, Cubano LA, Vlaar CP, Dharmawardhane S. Characterization of a Dual Rac/Cdc42 Inhibitor MBQ-167 in Metastatic Cancer. Mol Cancer Ther. 2017 05; 16(5):805-818.
PMID: 28450422.
Citations:
45 Fields:
Translation:
HumansAnimalsCells
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Rivera Rivera A, Castillo-Pichardo L, Gerena Y, Dharmawardhane S. Anti-Breast Cancer Potential of Quercetin via the Akt/AMPK/Mammalian Target of Rapamycin (mTOR) Signaling Cascade. PLoS One. 2016; 11(6):e0157251.
PMID: 27285995.
Citations:
43 Fields:
Translation:
HumansAnimalsCells
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de la Parra C, Castillo-Pichardo L, Cruz-Collazo A, Cubano L, Redis R, Calin GA, Dharmawardhane S. Soy Isoflavone Genistein-Mediated Downregulation of miR-155 Contributes to the Anticancer Effects of Genistein. Nutr Cancer. 2016; 68(1):154-64.
PMID: 26771440.
Citations:
45 Fields:
Translation:
HumansCells
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de la Parra C, Borrero-Garcia LD, Cruz-Collazo A, Schneider RJ, Dharmawardhane S. Equol, an isoflavone metabolite, regulates cancer cell viability and protein synthesis initiation via c-Myc and eIF4G. J Biol Chem. 2015 Mar 06; 290(10):6047-57.
PMID: 25593313.
Citations:
7 Fields:
Translation:
HumansAnimalsCells
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Humphries-Bickley T, Castillo-Pichardo L, Corujo-Carro F, Duconge J, Hernandez-O'Farrill E, Vlaar C, Rodriguez-Orengo JF, Cubano L, Dharmawardhane S. Pharmacokinetics of Rac inhibitor EHop-016 in mice by ultra-performance liquid chromatography tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci. 2015 Feb 15; 981-982:19-26.
PMID: 25594952.
Citations:
18 Fields:
Translation:
Animals
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Cekanova M, Fernando RI, Siriwardhana N, Sukhthankar M, Parra C, Woraratphoka J, Malone C, Str?m A, Baek SJ, Wade PA, Saxton AM, Donnell RM, Pestell RG, Dharmawardhane S, Wimalasena J. BCL-2 family protein, BAD is down-regulated in breast cancer and inhibits cell invasion. Exp Cell Res. 2015 Feb 01; 331(1):1-10.
PMID: 25499972.
Citations:
14 Fields:
Translation:
HumansCells
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Castillo-Pichardo L, Dharmawardhane S, Rodr?guez-Orengo JF. Rapid quantification of resveratrol in mouse plasma by ultra high pressure liquid chromatography (UPLC) coupled to tandem mass spectrometry. P R Health Sci J. 2014 Dec; 33(4):151-6.
PMID: 25563031.
Citations: Fields:
Translation:
AnimalsCells
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Castillo-Pichardo L, Humphries-Bickley T, De La Parra C, Forestier-Roman I, Martinez-Ferrer M, Hernandez E, Vlaar C, Ferrer-Acosta Y, Washington AV, Cubano LA, Rodriguez-Orengo J, Dharmawardhane S. The Rac Inhibitor EHop-016 Inhibits Mammary Tumor Growth and Metastasis in a Nude Mouse Model. Transl Oncol. 2014 Oct; 7(5):546-55.
PMID: 25389450.
Citations:
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Ramos G, Loperena Y, Ortiz G, Reyes F, Szeto A, Vera J, Velez J, Morales J, Morrero D, Castillo L, Dharmawardhane S, Melendez E, Washington AV. The addition of a pregnenolone pendant group enhances the anticancer properties of titanocene dichloride in a mcf-7 xenograft model. Anticancer Res. 2014 Apr; 34(4):1609-15.
PMID: 24692689.
Citations:
2 Fields:
Translation:
HumansAnimalsCells
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Martin H, Mali RS, Ma P, Chatterjee A, Ramdas B, Sims E, Munugalavadla V, Ghosh J, Mattingly RR, Visconte V, Tiu RV, Vlaar CP, Dharmawardhane S, Kapur R. Pak and Rac GTPases promote oncogenic KIT-induced neoplasms. J Clin Invest. 2013 Oct; 123(10):4449-63.
PMID: 24091327.
Citations:
28 Fields:
Translation:
HumansAnimalsCells
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Dharmawardhane S, Hernandez E, Vlaar C. Development of EHop-016: a small molecule inhibitor of Rac. Enzymes. 2013; 33 Pt A:117-46.
PMID: 25033803.
Citations:
19 Fields:
Translation:
HumansAnimals
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Castillo-Pichardo L, Cubano LA, Dharmawardhane S. Dietary grape polyphenol resveratrol increases mammary tumor growth and metastasis in immunocompromised mice. BMC Complement Altern Med. 2013 Jan 08; 13:6.
PMID: 23298290.
Citations:
21 Fields:
Translation:
AnimalsCells
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de la Parra C, Otero-Franqui E, Martinez-Montemayor M, Dharmawardhane S. The soy isoflavone equol may increase cancer malignancy via up-regulation of eukaryotic protein synthesis initiation factor eIF4G. J Biol Chem. 2012 Dec 07; 287(50):41640-50.
PMID: 23095751.
Citations:
11 Fields:
Translation:
HumansAnimalsCells
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Montalvo-Ortiz BL, Castillo-Pichardo L, Hern?ndez E, Humphries-Bickley T, De la Mota-Peynado A, Cubano LA, Vlaar CP, Dharmawardhane S. Characterization of EHop-016, novel small molecule inhibitor of Rac GTPase. J Biol Chem. 2012 Apr 13; 287(16):13228-38.
PMID: 22383527.
Citations:
123 Fields:
Translation:
HumansCells
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Castillo-Pichardo L, Dharmawardhane SF. Grape polyphenols inhibit Akt/mammalian target of rapamycin signaling and potentiate the effects of gefitinib in breast cancer. Nutr Cancer. 2012; 64(7):1058-69.
PMID: 23061908.
Citations:
26 Fields:
Translation:
HumansAnimalsCells
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Mart?nez-Montemayor MM, Acevedo RR, Otero-Franqui E, Cubano LA, Dharmawardhane SF. Ganoderma lucidum (Reishi) inhibits cancer cell growth and expression of key molecules in inflammatory breast cancer. Nutr Cancer. 2011; 63(7):1085-94.
PMID: 21888505.
Citations:
31 Fields:
Translation:
HumansAnimalsCells
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Hern?ndez E, De La Mota-Peynado A, Dharmawardhane S, Vlaar CP. Novel inhibitors of Rac1 in metastatic breast cancer. P R Health Sci J. 2010 Dec; 29(4):348-56.
PMID: 21261173.
Citations:
21 Fields:
Translation:
HumansCells
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Mart?nez-Montemayor MM, Otero-Franqui E, Martinez J, De La Mota-Peynado A, Cubano LA, Dharmawardhane S. Individual and combined soy isoflavones exert differential effects on metastatic cancer progression. Clin Exp Metastasis. 2010 Oct; 27(7):465-80.
PMID: 20517637.
Citations:
26 Fields:
Translation:
HumansAnimalsCells
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Castillo-Pichardo L, Mart?nez-Montemayor MM, Mart?nez JE, Wall KM, Cubano LA, Dharmawardhane S. Inhibition of mammary tumor growth and metastases to bone and liver by dietary grape polyphenols. Clin Exp Metastasis. 2009; 26(6):505-16.
PMID: 19294520.
Citations:
31 Fields:
Translation:
HumansAnimalsCells
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Schlachterman A, Valle F, Wall KM, Azios NG, Castillo L, Morell L, Washington AV, Cubano LA, Dharmawardhane SF. Combined resveratrol, quercetin, and catechin treatment reduces breast tumor growth in a nude mouse model. Transl Oncol. 2008 Mar; 1(1):19-27.
PMID: 18607509.
Citations:
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Calabria LM, Piacente S, Kapusta I, Dharmawardhane SF, Segarra FM, Pessiki PJ, Mabry TJ. Triterpene saponins from Silphium radula. Phytochemistry. 2008 Feb; 69(4):961-72.
PMID: 18039545.
Citations:
4 Fields:
Translation:
HumansAnimalsCells
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Azios NG, Krishnamoorthy L, Harris M, Cubano LA, Cammer M, Dharmawardhane SF. Estrogen and resveratrol regulate Rac and Cdc42 signaling to the actin cytoskeleton of metastatic breast cancer cells. Neoplasia. 2007 Feb; 9(2):147-58.
PMID: 17356711.
Citations:
39 Fields:
Translation:
HumansCells
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Sokolov K, Nida D, Descour M, Lacy A, Levy M, Hall B, Dharmawardhane S, Ellington A, Korgel B, Richards-Kortum R. Molecular optical imaging of therapeutic targets of cancer. Adv Cancer Res. 2007; 96:299-344.
PMID: 17161684.
Citations:
8 Fields:
Translation:
HumansAnimals
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Carlson AL, Hoffmeyer MR, Wall KM, Baugher PJ, Richards-Kortum R, Dharmawardhane SF. In situ analysis of breast cancer progression in murine models using a macroscopic fluorescence imaging system. Lasers Surg Med. 2006 Dec; 38(10):928-38.
PMID: 17111410.
Citations:
8 Fields:
Translation:
AnimalsCells
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Baugher PJ, Krishnamoorthy L, Price JE, Dharmawardhane SF. Rac1 and Rac3 isoform activation is involved in the invasive and metastatic phenotype of human breast cancer cells. Breast Cancer Res. 2005; 7(6):R965-74.
PMID: 16280046.
Citations:
59 Fields:
Translation:
HumansCells
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Hoffmeyer MR, Wall KM, Dharmawardhane SF. In vitro analysis of the invasive phenotype of SUM 149, an inflammatory breast cancer cell line. Cancer Cell Int. 2005 Apr 27; 5(1):11.
PMID: 15857504.
Citations:
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Azios NG, Dharmawardhane SF. Resveratrol and estradiol exert disparate effects on cell migration, cell surface actin structures, and focal adhesion assembly in MDA-MB-231 human breast cancer cells. Neoplasia. 2005 Feb; 7(2):128-40.
PMID: 15802018.
Citations:
31 Fields:
Translation:
HumansCells
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Hsu ER, Anslyn EV, Dharmawardhane S, Alizadeh-Naderi R, Aaron JS, Sokolov KV, El-Naggar AK, Gillenwater AM, Richards-Kortum RR. A far-red fluorescent contrast agent to image epidermal growth factor receptor expression. Photochem Photobiol. 2004 Mar; 79(3):272-9.
PMID: 15115300.
Citations:
11 Fields:
Translation:
HumansCells
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Brownson DM, Azios NG, Fuqua BK, Dharmawardhane SF, Mabry TJ. Flavonoid effects relevant to cancer. J Nutr. 2002 11; 132(11 Suppl):3482S-3489S.
PMID: 12421874.
Citations:
25 Fields:
Translation:
HumansCells
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Lacy AA, Collier T, Price JE, Dharmawardhane S, Richards-Kortum R. Near real-time in vivo confocal imaging of mouse mammary tumors. Front Biosci. 2002 Jan 01; 7:f1-7.
PMID: 11779701.
Citations:
1 Fields:
Translation:
HumansAnimals
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Year | Publications |
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2002 | 2 |
2004 | 1 |
2005 | 3 |
2006 | 1 |
2007 | 3 |
2008 | 1 |
2009 | 1 |
2010 | 2 |
2011 | 1 |
2012 | 3 |
2013 | 3 |
2014 | 4 |
2015 | 2 |
2016 | 2 |
2017 | 2 |
2018 | 2 |
2019 | 3 |
2020 | 3 |
2021 | 4 |
2022 | 1 |
2023 | 2 |
2024 | 2 |
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