David R. Entenberg

David R. Entenberg, Ph.D.

  • Associate Professor, Department of Pathology
  • Co-Director, Gruss-Lipper Biophotonics Center
  • Director of Technology Development, Integrated Imaging Program
  • Director of Integrated Imaging, Integrated Imaging Program
  • Leader, Computational Analysis of Biomarkers Program, Integrated Imaging Program for Cancer Research

Area of research

  • Development of photonics based assays for metastasis research. Specific areas of focus include: intravital imaging, quantitative digital pathology, biomarker development and validation, and surgical engineering.

Email

Phone

Location

  • Albert Einstein College of Medicine Michael F. Price Center 1301 Morris Park Avenue 208 Bronx, NY 10461

Lab of David R. Entenberg



Professional Interests

David Entenberg’s research interests are in the development of enabling technologies for biological research. With a background in laser based experimental quantum physics he brings skills in optical, mechanical, electrical, software and instrument design to biological research. Previous work has included the design and development of several robotics-based high-throughput automated biological assays utilizing real time PCR and MALDI-TOF protocols, novel microscopes including a fast switching, multi-channel TIRF microscope, a video rate multiphoton microscope, and a two-laser, OPO based multiphoton microscope. Current projects are focused on utilizing surgical engineering to develop and validate techniques for expanding the utility of mouse models within intravital imaging. This work has included mammary, abdominal, brain, lymphatic and lung imaging windows for studying cancer metastasis to secondary sites in vivo, as well surgically implantable photolithographic microdevices designed to directly alter the local (<300um) microenvironment in vivo and during intravital imaging.

He has authored several book chapters on multiphoton microscopy and intravital imaging and is co-Director of Einstein’s Quantitative Imaging of Cells course. He currently serves as co-Director of Einstein's Gruss Lipper Biophotonics Center, Director of Technological Development within the Integrated Imaging Program, and Leader of the Computational Analysis of Biomarkers Program within the Integrated Imaging Program for Cancer Research.

Selected Publications

My Bibliography

  1. Scheele CL, Herrmann D, Yamashita E, Lo Celso C, Jenne CN, Oktay MH, Entenberg D, Friedl P, Weigert R, Meijboom FL. Multiphoton intravital microscopy of rodents. Nature Reviews Methods Primers. 2022;2(1):1-26.51.    Ye X, Oktay MH, Xue X, Rohan TE, Ginter PS, D'Alfonso T, Kornaga EN, Morris DG, Entenberg D, Condeelis JS. Combining TMEM Doorway Score and Mena(Calc) Score Improves the Prediction of Distant Recurrence Risk in HR+/HER2- Breast Cancer Patients. Cancers (Basel). 2022;14(9). Epub 20220426. doi: 10.3390/cancers14092168. PubMed PMID: 35565297; PMCID: PMC9101795
  2. Selvanesan BC, Chandra D, Quispe-Tintaya W, Jahangir A, Patel A, Meena K, Alves Da Silva RA, Friedman M, Gabor L, Khouri O, Libutti SK, Yuan Z, Li J, Siddiqui S, Beck A, Tesfa L, Koba W, Chuy J, McAuliffe JC, Jafari R, Entenberg D, Wang Y, Condeelis J, DesMarais V, Balachandran V, Zhang X, Lin K, Gravekamp C. Listeria delivers tetanus toxoid protein to pancreatic tumors and induces cancer cell death in mice. Sci Transl Med. 2022;14(637):eabc1600. Epub 20220323. doi: 10.1126/scitranslmed.abc1600. PubMed PMID: 35320003; PMCID: PMC9031812.
  3. Rodriguez-Tirado C, Entenberg D, Li J, Qian BZ, Condeelis JS, Pollard JW. Interleukin 4 Controls the Pro-Tumoral Role of Macrophages in Mammary Cancer Pulmonary Metastasis in Mice. Cancers (Basel). 2022;14(17). Epub 20220905. doi: 10.3390/cancers14174336. PubMed PMID: 36077870.
  4. Kim G, Pastoriza JM, Qin J, Lin J, Karagiannis GS, Condeelis JS, Yothers G, Anderson S, Julian T, Entenberg D, Rohan TE, Xue X, Sparano JA, Oktay MH. Racial disparity in distant recurrence-free survival in patients with localized breast cancer: A pooled analysis of National Surgical Adjuvant Breast and Bowel Project trials. Cancer. 2022;128(14):2728-35. Epub 20220517. doi: 10.1002/cncr.34241. PubMed PMID: 35578919.
  5. Du W, Adkisson C, Ye X, Duran CL, Chellakkan Selvanesan B, Gravekamp C, Oktay MH, McAuliffe JC, Condeelis JS, Panarelli NC, Norgard RJ, Sela Y, Stanger BZ, Entenberg D. SWIP-a stabilized window for intravital imaging of the murine pancreas. Open Biol. 2022;12(6):210273. Epub 20220615. doi: 10.1098/rsob.210273. PubMed PMID: 35702996.
  6. Borriello L, Coste A, Traub B, Sharma VP, Karagiannis GS, Lin Y, Wang Y, Ye X, Duran CL, Chen X, Friedman M, Sosa MS, Sun D, Dalla E, Singh DK, Oktay MH, Aguirre-Ghiso JA, Condeelis JS, Entenberg D. Primary tumor associated macrophages activate programs of invasion and dormancy in disseminating tumor cells. Nat Commun. 2022;13(1):626. Epub 2022/02/04. doi: 10.1038/s41467-022-28076-3. PubMed PMID: 35110548; PMCID: PMC8811052.
  7. Sharma VP, Tang B, Wang Y, Duran CL, Karagiannis GS, Xue EA, Entenberg D, Borriello L, Coste A, Eddy RJ, Kim G, Ye X, Jones JG, Grunblatt E, Agi N, Roy S, Bandyopadhyaya G, Adler E, Surve CR, Esposito D, Goswami S, Segall JE, Guo W, Condeelis JS, Wakefield LM, Oktay MH. Live tumor imaging shows macrophage induction and TMEM-mediated enrichment of cancer stem cells during metastatic dissemination. Nat Commun. 2021;12(1):7300. Epub 2021/12/17. doi: 10.1038/s41467-021-27308-2. PubMed PMID: 34911937; PMCID: PMC8674234.
  8. Sharma VP, Williams J, Leung E, Sanders J, Eddy R, Castracane J, Oktay MH, Entenberg D, Condeelis JS. SUN-MKL1 Crosstalk Regulates Nuclear Deformation and Fast Motility of Breast Carcinoma Cells in Fibrillar ECM Microenvironment. Cells. 2021;10(6). Epub 2021/07/03. doi: 10.3390/cells10061549. PubMed PMID: 34205257; PMCID: PMC8234170.
  9. Borriello L, Condeelis J, Entenberg D, Oktay MH. Breast Cancer Cell Re-Dissemination from Lung Metastases-A Mechanism for Enhancing Metastatic Burden. J Clin Med. 2021;10(11). Epub 2021/06/03. doi: 10.3390/jcm10112340. PubMed PMID: 34071839; PMCID: PMC8199463.
  10. Borriello L, Traub B, Coste A, Oktay MH, Entenberg D. A Permanent Window for Investigating Cancer Metastasis to the Lung. J Vis Exp. 2021(173). Epub 2021/07/20. doi: 10.3791/62761. PubMed PMID: 34279505
  11. Shanja-Grabarz X, Coste A, Entenberg D, Di Cristofano A. Real-time, high-resolution imaging of tumor cells in genetically engineered and orthotopic models of thyroid cancer. Endocrine-related cancer. 2020;27(10):529-39. Epub 2020/07/23. doi: 10.1530/ERC-20-0295. PubMed PMID: 32698130.
  12. Entenberg D, Oktay MH, D'Alfonso T, Ginter PS, Robinson BD, Xue X, Rohan TE, Sparano JA, Jones JG, Condeelis JS. Validation of an Automated Quantitative Digital Pathology Approach for Scoring TMEM, a Prognostic Biomarker for Metastasis. Cancers (Basel). 2020;12(4). Epub 2020/04/05. doi: 10.3390/cancers12040846. PubMed PMID: 32244564; PMCID: PMC7226227.
  13. Coste A, Karagiannis GS, Wang Y, Xue EA, Lin Y, Skobe M, Jones JG, Oktay MH, Condeelis JS, Entenberg D. Hematogenous Dissemination of Breast Cancer Cells From Lymph Nodes Is Mediated by Tumor MicroEnvironment of Metastasis Doorways. Front Oncol. 2020;10:571100. Epub 2020/11/17. doi: 10.3389/fonc.2020.571100. PubMed PMID: 33194666; PMCID: PMC7649363.
  14. Sanchez LR, Borriello L, Entenberg D, Condeelis JS, Oktay MH, Karagiannis GS. The emerging roles of macrophages in cancer metastasis and response to chemotherapy. J Leukoc Biol. 2019;106(2):259-74. Epub 2019/02/06. doi: 10.1002/JLB.MR0218-056RR. PubMed PMID: 30720887; PMCID: PMC6779158.
  15. Entenberg D, Oktay MH, D'Alfonso T, Ginter PS, Robinson BD, Xue X, Rohan TE, Sparano JA, Jones JG, Condeelis JS. Validation of an Automated Quantitative Digital Pathology Approach for Scoring TMEM, a Prognostic Biomarker for Metastasis. Cancers (Basel). 2020;12(4). Epub 2020/04/05. doi: 10.3390/cancers12040846. PubMed PMID: 32244564.
  16. Ginter PS, Karagiannis GS, Entenberg D, Lin Y, Condeelis J, Jones JG, Oktay MH. Tumor Microenvironment of Metastasis (TMEM) Doorways Are Restricted to the Blood Vessel Endothelium in Both Primary Breast Cancers and Their Lymph Node Metastases. Cancers (Basel). 2019;11(10). Epub 2019/10/11. doi: 10.3390/cancers11101507. PubMed PMID: 31597373.
  17. Karagiannis GS, Pastoriza JM, Borriello L, Jafari R, Coste A, Condeelis JS, Oktay MH, Entenberg D. Assessing Tumor Microenvironment of Metastasis Doorway-Mediated Vascular Permeability Associated with Cancer Cell Dissemination using Intravital Imaging and Fixed Tissue Analysis. Journal of visualized experiments : JoVE. 2019(148). Epub 2019/07/16. doi: 10.3791/59633. PubMed PMID: 31305525.
  18. Liu X, Taftaf R, Kawaguchi M, Chang YF, Chen W, Entenberg D, Zhang Y, Gerratana L, Huang S, Patel DB, Tsui E, Adorno-Cruz V, Chirieleison SM, Cao Y, Harney AS, Patel S, Patsialou A, Shen Y, Avril S, Gilmore HL, Lathia JD, Abbott DW, Cristofanilli M, Condeelis JS, Liu H. Homophilic CD44 Interactions Mediate Tumor Cell Aggregation and Polyclonal Metastasis in Patient-Derived Breast Cancer Models. Cancer Discov. 2019;9(1):96-113. Epub 2018/10/27. doi: 10.1158/2159-8290.CD-18-0065. PubMed PMID: 30361447; PMCID: PMC6328322.
  19. Pastoriza JM, Karagiannis GS, Lin J, Lanjewar S, Entenberg D, Condeelis JS, Sparano JA, Xue X, Rohan TE, Oktay MH. Black race and distant recurrence after neoadjuvant or adjuvant chemotherapy in breast cancer. Clin Exp Metastasis. 2018. Epub 2018/08/24. doi: 10.1007/s10585-018-9932-8. PubMed PMID: 30136072.
  20. Nobre AR, Entenberg D, Wang Y, Condeelis J, Aguirre-Ghiso JA. The Different Routes to Metastasis via Hypoxia-Regulated Programs. Trends Cell Biology. 2018. Epub 2018/07/26. doi: 10.1016/j.tcb.2018.06.008. PubMed PMID: 30041830.
  21. Entenberg D, Voiculescu S, Guo P, Borriello L, Wang Y, Karagiannis GS, Jones J, Baccay F, Oktay M, Condeelis J. A permanent window for the murine lung enables high-resolution imaging of cancer metastasis. Nature Methods. 2018;15(1):73-80. Epub 2017/11/28. doi: 10.1038/nmeth.4511. PubMed PMID: 29176592; PMCID: 5755704.
  22. Arwert EN, Harney AS, Entenberg D, Wang Y, Sahai E, Pollard JW, Condeelis JS. A Unidirectional Transition from Migratory to Perivascular Macrophage Is Required for Tumor Cell Intravasation. Cell Rep. 2018;23(5):1239-48. doi: 10.1016/j.celrep.2018.04.007. PubMed PMID: 29719241; PMCID: 5946803.
  23. Sparano JA, Gray R, Oktay MH, Entenberg D, Rohan T, Xue X, Donovan M, Peterson M, Shuber A, Hamilton DA, D'Alfonso T, Goldstein LJ, Gertler F, Davidson NE, Condeelis J, Jones J. A metastasis biomarker (MetaSite Breast Score) is associated with distant recurrence in hormone receptor-positive, HER2-negative early-stage breast cancer. Nature PJ Breast Cancer. 2017;3:42. doi: 10.1038/s41523-017-0043-5. PubMed PMID: 29138761; PMCID: 5678158.
  24. Entenberg D, Pastoriza JM, Oktay MH, Voiculescu S, Wang Y, Sosa MS, Aguirre-Ghiso J, Condeelis J. Time-lapsed, large-volume, high-resolution intravital imaging for tissue-wide analysis of single cell dynamics. Methods. 2017;128:65-77. doi: 10.1016/j.ymeth.2017.07.019. PubMed PMID: 28911733; PMCID: 5659295.
  25. Karagiannis GS, Pastoriza JM, Wang Y, Harney AS, Entenberg D, Pignatelli J, Sharma VP, Xue EA, Cheng E, D'Alfonso TM, Jones JG, Anampa J, Rohan TE, Sparano JA, Condeelis JS, Oktay MH. (2017). Neoadjuvant chemotherapy induces breast cancer metastasis through a TMEM-mediated mechanism. Science Translational Medicine. 9(397). PMID: 28679654.
  26. Fluegen G, Avivar-Valderas A, Wang Y, Padgen MR, Williams JK, Nobre AR, Calvo V, Cheung JF, Bravo-Cordero JJ, Entenberg D, Castracane J, Verkhusha V, Keely PJ, Condeelis J, Aguirre-Ghiso JA. (2017). Phenotypic heterogeneity of disseminated tumour cells is preset by primary tumour hypoxic microenvironments. Nature Cell Biology. PMID: 28114271.
  27. Williams JK, Entenberg D, Wang Y, Avivar-Valderas A, Padgen M, Clark A, Aguirre-Ghiso JA, Castracane J, Condeelis JS. (2016). Validation of a device for the active manipulation of the tumor microenvironment during intravital imaging. Intravital. 5(2). PMID: 27790386 / PMCID: PMCPMC5079288. (Co-First Author Publication)
  28. Wang Y, Wang H, Li J, Entenberg D, Xue A, Wang W, Condeelis J. (2016). Direct visualization of the phenotype of hypoxic tumor cells at single cell resolution in vivo using a new hypoxia probe. Intravital. 5(2). PMID: 27790387 / PMCID: PMCPMC5079291.
  29. Szulczewski JM, Inman DR, Entenberg D, Ponik SM, Aguirre-Ghiso J, Castracane J, Condeelis J, Eliceiri KW, Keely PJ. (2016). In Vivo Visualization of Stromal Macrophages via label-free FLIM-based metabolite imaging. Scientific Reports. 6:25086. PMID: 27220760 / PMCID: PMCPMC4879594.
  30. Rodriguez-Tirado C, Kitamura T, Kato Y, Pollard JW, Condeelis JS, Entenberg D. (2016). Long-term High-Resolution Intravital Microscopy in the Lung with a Vacuum Stabilized Imaging Window. Journal of Visualized Experiments. (116):e54603. PMID: 27768066.
  31. Harper KL, Sosa MS, Entenberg D, Hosseini H, Cheung JF, Nobre R, Avivar-Valderas A, Nagi C, Girnius N, Davis RJ, Farias EF, Condeelis J, Klein CA, Aguirre-Ghiso JA. (2016). Mechanism of early dissemination and metastasis in Her2+ mammary cancer. Nature. PMID: 27974798.
  32. Harney AS, Wang Y, Condeelis JS, Entenberg D. (2016). Extended Time-lapse Intravital Imaging of Real-time Multicellular Dynamics in the Tumor Microenvironment. Journal of Visualized Experiments. (112):e54042. PMID: 27341448 / PMCID: PMCPMC4927790.
  33. Zolla V, Nizamutdinova IT, Scharf B, Clement CC, Maejima D, Akl T, Nagai T, Luciani P, Leroux JC, Halin C, Stukes S, Tiwari S, Casadevall A, Jacobs WR, Jr., Entenberg D, Zawieja DC, Condeelis J, Fooksman DR, Gashev AA, Santambrogio L. (2015). Aging-related anatomical and biochemical changes in lymphatic collectors impair lymph transport, fluid homeostasis, and pathogen clearance. Aging Cell. 14(4):582-94. PMID: 25982749 / PMCID: PMC4531072.
  34. Patsialou A, Wang Y, Pignatelli J, Chen X, Entenberg D, Oktay M, Condeelis JS. (2015). Autocrine CSF1R signaling mediates switching between invasion and proliferation downstream of TGFbeta in claudin-low breast tumor cells. Oncogene. PMID: 25088194 / PMCID: PMC25088194
  35. Lim SJ, Zahid MU, Le P, Ma L, Entenberg D, Harney AS, Condeelis J, Smith AM. (2015). Brightness-equalized quantum dots. Nature Communications. 6:8210. PMID: 26437175 / PMCID: PMC4594210.
  36. Harney AS, Arwert EN, Entenberg D, Wang Y, Guo P, Qian BZ, Oktay MH, Pollard JW, Jones JG, Condeelis JS. (2015). Real-Time Imaging Reveals Local, Transient Vascular Permeability, and Tumor Cell Intravasation Stimulated by TIE2hi Macrophage-Derived VEGFA. Cancer Discovery. 5(9):932-43. PMID: 26269515 / PMCID: PMC4560669.
  37. Entenberg D, Rodriguez-Tirado C, Kato Y, Kitamura T, Pollard JW, Condeelis J. (2015). Subcellular resolution optical imaging in the lung reveals early metastatic proliferation and motility. Intravital. 4(3). PMID: 26855844 / PMCID: PMC4737962.
  38. Sharma VP, Entenberg D, Condeelis J. (2013). High-resolution live-cell imaging and time-lapse microscopy of invadopodium dynamics and tracking analysis. Methods in Molecular Biology. 1046:343-57. PMID: 23868599 / PMCID: PMC3933219.
  39. Sharma VP, Eddy R, Entenberg D, Kai M, Gertler FB, Condeelis J. (2013). Tks5 and SHIP2 regulate invadopodium maturation, but not initiation, in breast carcinoma cells. Current Biology. 23(21):2079-89. PMID: 24206842 / PMCID: PMC3882144.
  40. Patsialou A, Bravo-Cordero JJ, Wang Y, Entenberg D, Liu H, Clarke M, Condeelis JS. (2013). Intravital multiphoton imaging reveals multicellular streaming as a crucial component of in vivo cell migration in human breast tumors. Intravital. 2(2):e25294. PMID: 25013744 / PMCID: PMC3908591.
  41. Entenberg D, Kedrin D, Wyckoff J, Sahai E, Condeelis J, Segall JE. (2013). Imaging tumor cell movement in vivo. Current Protocols in Cell Biology. Chapter 19:Unit19 7. PMID: 23456602 / PMCID: PMC3722061.
  42. Das S, Sarrou E, Podgrabinska S, Cassella M, Mungamuri SK, Feirt N, Gordon R, Nagi CS, Wang Y, Entenberg D, Condeelis J, Skobe M. (2013). Tumor cell entry into the lymph node is controlled by CCL1 chemokine expressed by lymph node lymphatic sinuses. Journal of Experimental Medicine. 210(8):1509-28. PMID: 23878309 / PMCID: PMC3727324.
  43. Subach OM, Entenberg D, Condeelis JS, Verkhusha VV. (2012). A FRET-facilitated photoswitching using an orange fluorescent protein with the fast photoconversion kinetics. Journal of the American Chemical Society. 134(36):14789-99. PMID: 22900938 / PMCID: PMC3444247.
  44. Hulit J, Kedrin D, Gligorijevic B, Entenberg D, Wyckoff J, Condeelis J, Segall JE. (2012). The use of fluorescent proteins for intravital imaging of cancer cell invasion. Methods in Molecular Biology. 872:15-30. PMID: 22700401 / PMCID: PMC4000026.
  45. Wyckoff J, Gligorijevic B, Entenberg D, Segall J, Condeelis J. (2011). High-resolution multiphoton imaging of tumors in vivo. Cold Spring Harb Protoc. 2011(10):1167-84. PMID: 21969629.
  46. Wyckoff J, Gligorijevic B, Entenberg D, Segall J, Condeelis J. (2011). The in vivo invasion assay: preparation and handling of collection needles. Cold Spring Harb Protoc. 2011(10):1232-4. PMID: 21969630.
  47. Entenberg D, Wyckoff J, Gligorijevic B, Roussos ET, Verkhusha VV, Pollard JW, Condeelis J. (2011). Setup and use of a two-laser multiphoton microscope for multichannel intravital fluorescence imaging. Nature protocols. 6(10):1500-20. PMID: 21959234.
  48. Dovas A, Gligorijevic B, Chen X, Entenberg D, Condeelis J, Cox D. (2011). Visualization of actin polymerization in invasive structures of macrophages and carcinoma cells using photoconvertible beta-actin-Dendra2 fusion proteins. PloS one. 6(2):e16485. PMID: 21339827 / PMCID: PMC3038862.
  49. Wyckoff J, Gligorijevic B, Entenberg D, Segall JE, Condeelis J. (2010). High-Resolution multiphoton imaging of Tumors in vivo. Live Cell Imaging: A Laboratory Manual.441-61. / PMCID: PMC4000043.
  50. Gligorijevic B, Entenberg D, Kedrin D, Segall J, van Rheenen J, Condeelis J. (2010). Intravital Imaging and Photoswitching in Tumor Invasion and Intravasation Microenvironments. Micros Today. 18(1):34-7. PMID: 25635177 / PMCID: PMC4307802.
  51. Gligorijevic B, Entenberg D, Kedrin D, Segall J, van Rheenen J, Condeelis J. (2009). Intravital imaging and photoswitching in tumor invasion and intravasation microenvironments. Microscopy and Microanalysis. Supplement 2(15):86-7.
  52. Dunphy MP, Entenberg D, Toledo-Crow R, Larson SM. (2009). In vivo microcartography and subcellular imaging of tumor angiogenesis: a novel platform for translational angiogenesis research. Microvascular research. 78(1):51-6. PMID: 19362098 / PMCID: PMC2739383.
  53. Entenberg D, Aranda I, Li Y, Toledo-Crow R, Schaer D, Li Y. (2006). Multimodal microscopy of immune cells and melanoma for longitudinal studies. Proc of SPIE. 6081:62-73.
  54. Villanueva J, Philip J, Entenberg D, Chaparro CA, Tanwar MK, Holland EC, Tempst P. (2004). Serum peptide profiling by magnetic particle-assisted, automated sample processing and MALDI-TOF mass spectrometry. Analytical chemistry. 76(6):1560-70. PMID: 15018552.
  55. Entenberg D, Roorda RD, Toledo-Crow R. Non-linear microscope for imaging of the neural systems in live drosophila. OSA BioMed 2004.