Research Highlights

Background: Mitochondrial dynamics underlies malignant transformation, cancer progression, and response to treatment. Current research presents conflicting evidence for functions of mitochondrial fission and fusion in tumor progression. Here, we investigated how mitochondrial fission and fusion states regulate underlying processes of cancer progression and metastasis in triple-negative breast cancer (TNBC).

Methods: We enforced mitochondrial fission and fusion states through chemical or genetic approaches and measured migration and invasion of TNBC cells in 2D and 3D in vitro models. We also utilized kinase translocation reporters (KTRs) to identify single cell effects of mitochondrial state on signaling cascades, PI3K/Akt/mTOR and Ras/Raf/MEK/ERK, commonly activated in TNBC. Furthermore, we determined effects of fission and fusion states on metastasis, bone destruction, and signaling in mouse models of breast cancer.

Results: Enforcing mitochondrial fission through chemical or genetic approaches inhibited migration, invasion, and metastasis in TNBC. Breast cancer cells with predominantly fissioned mitochondria exhibited reduced activation of Akt and ERK both in vitro and in mouse models of breast cancer. Treatment with leflunomide, a potent activator of mitochondrial fusion proteins, overcame inhibitory effects of fission on migration, signaling, and metastasis. Mining existing datasets for breast cancer revealed that increased expression of genes associated with mitochondrial fission correlated with improved survival in human breast cancer.

Conclusions: In TNBC, mitochondrial fission inhibits cellular processes and signaling pathways associated with cancer progression and metastasis. These data suggest that therapies driving mitochondrial fission may benefit patients with breast cancer.

Abstract: Migration and invasion of cancer cells constitute fundamental processes in tumor progression and metastasis. Migratory cancer cells commonly upregulate expression of plasminogen activator inhibitor 1 (PAI1), and PAI1 correlates with poor prognosis in breast cancer. However, mechanisms by which PAI1 promotes migration of cancer cells remain incompletely defined. Here we show that increased PAI1 drives rearrangement of the actin cytoskeleton, mitochondrial fragmentation, and glycolytic metabolism in triple negative breast cancer (TNBC) cells. In two-dimensional environments, both stable expression of PAI1 and treatment with recombinant PAI1 increased migration, which could be blocked with the specific inhibitor tiplaxtinin. PAI1 also promoted invasion into the extracellular matrix from co-culture spheroids with human mammary fibroblasts in fibrin gels. Elevated cellular PAI1 enhanced cytoskeletal features associated with migration, actin-rich migratory structures and reduced actin stress fibers. In orthotopic tumor xenografts, we discovered that TNBC cells with elevated PAI1 show collagen fibers aligned perpendicular to the tumor margin, an established marker of invasive breast tumors. Further studies revealed that PAI1 activates ERK signaling, a central regulator of motility, and promotes mitochondrial fragmentation. Consistent with known effects of mitochondrial fragmentation on metabolism, fluorescence lifetime imaging microscopy (FLIM) of endogenous NADH showed that PAI1 promotes glycolysis in cell-based assays, orthotopic tumor xenografts, and lung metastases. Together, these data demonstrate for the first time that PAI1 regulates cancer cell metabolism and suggest targeting metabolism to block motility and tumor progression. Implications: We identified a novel mechanism through which cancer cells alter their metabolism to promote tumor progression.

Abstract: Estrogen receptor-positive (ER+) breast cancer can recur up to 20 years after initial diagnosis. Delayed recurrences arise from disseminated tumors cells (DTCs) in sites such as bone marrow that remain quiescent during endocrine therapy and subsequently proliferate to produce clinically detectable metastases. Identifying therapies that eliminate DTCs and/or effectively target cells transitioning to proliferation promises to reduce risk of recurrence. To tackle this problem, we utilized a 3D co-culture model incorporating ER+ breast cancer cells and bone marrow mesenchymal stem cells to represent DTCs in a bone marrow niche. 3D co-cultures maintained cancer cells in a quiescent, viable state as measured by both single-cell and population-scale imaging. Single-cell imaging methods for metabolism by fluorescence lifetime (FLIM) of NADH and signaling by kinases Akt and ERK revealed that breast cancer cells utilized oxidative phosphorylation and signaling by Akt to a greater extent both in 3D co-cultures and a mouse model of ER+ breast cancer cells in bone marrow. Using our 3D co-culture model, we discovered that combination therapies targeting oxidative phosphorylation via the thioredoxin reductase (TrxR) inhibitor, D9, and the Akt inhibitor, MK-2206, preferentially eliminated breast cancer cells without altering viability of bone marrow stromal cells. Treatment of mice with disseminated ER+ human breast cancer showed that D9 plus MK-2206 blocked formation of new metastases more effectively than tamoxifen. These data establish an integrated experimental system to investigate DTCs in bone marrow and identify combination therapy against metabolic and kinase targets as a promising approach to effectively target these cells and reduce risk of recurrence in breast cancer.

Abstract: The chemokine receptor CXCR4 regulates fundamental processes in development, normal physiology, and diseases, including cancer. Small subpopulations of CXCR4-positive cells drive the local invasion and dissemination of malignant cells during metastasis, emphasizing the need to understand the mechanisms controlling responses at the single-cell level to receptor activation by the chemokine ligand CXCL12. Using single-cell imaging, we discovered that short-term cellular memory of changes in environmental conditions tuned CXCR4 signaling to Akt and ERK, two kinases activated by this receptor. Conditioning cells with growth stimuli before CXCL12 exposure increased the number of cells that initiated CXCR4 signaling and the amplitude of Akt and ERK activation. Data-driven, single-cell computational modeling revealed that growth factor conditioning modulated CXCR4-dependent activation of Akt and ERK by decreasing extrinsic noise (preexisting cell-to-cell differences in kinase activity) in PI3K and mTORC1. Modeling established mTORC1 as critical for tuning single-cell responses to CXCL12-CXCR4 signaling. Our single-cell model predicted how combinations of extrinsic noise in PI3K, Ras, and mTORC1 superimposed on different driver mutations in the ERK and/or Akt pathways to bias CXCR4 signaling. Computational experiments correctly predicted that selected kinase inhibitors used for cancer therapy shifted subsets of cells to states that were more permissive to CXCR4 activation, suggesting that such drugs may inadvertently potentiate pro-metastatic CXCR4 signaling. Our work establishes how changing environmental inputs modulate CXCR4 signaling in single cells and provides a framework to optimize the development and use of drugs targeting this signaling pathway.


  1. Spinosa PC, Kinnunen PC, Humphries BA, Luker GD, Luker KE, Linderman JJ. Pre-existing Cell States Control Heterogeneity of Both EGFR and CXCR4 Signaling, Cell Mol Bioeng. 2020. PMID: 33643466

  2. Johanna M. Buschhaus, Brock A. Humphries, Samantha S. Eckley, Tanner H. Robison, Alyssa C. Cutter, Shrila Rajendran, Henry R. Haley, Avinash S. Bevoor, Kathryn E. Luker & Gary D. Luker. Targeting disseminated estrogen-receptor-positive breast cancer cells in bone marrow, Oncogene. 2020. PMID: 32678295.

  3. Humphries BA, Cutter AC, Buschhaus JM, Chen YC, Qyli T, Palagama DSW, Eckley S, Robison TH, Bevoor A, Chiang B, Haley HR, Sahoo S, Spinosa PC, Neale DB, Boppisetti J, Sahoo D, Ghosh P, Lahann J, Ross BD, Yoon E, Luker KE, Luker GD. Enhanced Mitochondrial Fission Suppresses Signaling and Metastasis in Triple-Negative Breast Cancer, Breast Cancer Research. 2020. PMID: 32503622.

  4. Singh S, Ray LA, Shahi Thakuri P, Tran S, Konopka MC, Luker GD, Tavana H. Organotypic Breast Tumor Model Elucidates Dynamic Remodeling of Tumor Microenvironment. Biomaterials. 2020. PMID: 32062146.

  5. El-Zaatari M, Bishu S, Zhang M, Grasberger H, Hou G, Haley H, Humphries B, Syu LJ, Dlugosz AA, Luker K, Luker GD, Eaton K, Kamada N, Cascalho M, Kao JY. Aim2-mediated/IFN-β-independent Regulation of Gastric Metaplastic Lesions via CD8+ T Cells. JCI Insight. 2020. PMID: 32053518

  6. Shahi Thakuri P, Gupta M, Singh S, Joshi R, Glasgow E, Lekan A, Agarwal S, Luker GD, Tavana H. Phytochemicals inhibit migration of triple negative breast cancer cells by targeting kinase signaling. BMC Cancer. 2020. PMID: 31898540

  7. Eckley SS, Buschhaus JM, Humphries BA, Robison TH, Luker KE, Luker GD: Short-Term Environmental Conditioning Enhances Tumorigenic Potential of Triple-Negative Breast Cancer Cells. Tomography: 2019. PMID: 31893233

  8. Chen YC , Sahoo S , Brien R , Jung S , Humphries B , Lee W , Cheng YH , Zhang Z , Luker KE , Wicha MS , Luker GD , Yoon E : Single-cell RNA-sequencing of migratory breast cancer cells: discovering genes associated with cancer metastasis. Analyst: 2019. PM31710321

  9. Jordahl S, Solorio L, Neale DB, McDermott S, Jordahl JH, Fox A, Dunlay C, Xiao A, Brown M, Wicha M, Luker GD, Lahann J: Engineered Fibrillar Fibronectin Networks as Three-Dimensional Tissue Scaffolds. Advanced Materials: 2019. PM31565823

  10. Spinosa PC, Humphries BA, Lewin Mejia D, Buschhaus JM, Linderman JJ, Luker GD, Luker KE: Short-term cellular memory tunes the signaling responses of the chemokine receptor CXCR4. Sci Signal: 2019. PM31289212

  11. Heureaux-Torres J, Luker KE, Haley H, Pirone M, Lee LM, Herrera Y, Luker GD, Liu AP: The effect of mechanosensitive channel MscL expression in cancer cells on 3D confined migration. APL Bioeng: 2018. PM31069318

  12. Rosenberg EM Jr, Harrison RES, Tsou LK, Drucker N, Humphries B, Rajasekaran D, Luker KE, Wu CH, Song JS, Wang CJ, Murphy JW, Cheng YC, Shia KS, Luker GD, Morikis D, Lolis EJ: Characterization, Dynamics, and Mechanism of CXCR4 Antagonists on a Constitutively Active Mutant. Cell Chem Biol:2019. PM30827936

  13. Humphries BA, Buschhaus JM, Chen YC, Haley HR, Qyli T, Chiang B, Shen N, Rajendran S, Cutter A, Cheng YH, Chen YT, Cong J, Spinosa PC, Yoon E, Luker KE, Luker GD: Plasminogen Activator Inhibitor 1 (PAI1) Promotes Actin Cytoskeleton Reorganization and Glycolytic Metabolism in Triple-Negative Breast Cancer. Mol Cancer Res: 2019. PM30718260

  14. Roseland ME, Kazerooni EA, Bailey JE, Luker GD, Cohan RH, Davenport MS: Needs Assessment Using a Structured Prioritization Schema: An Open Letter to PACS Vendors. J Am Coll Radiol 16(2): 170-177, 2019. PM30219343

  15. Liu C, Chiang B, Lewin Mejia D, Luker KE, Luker GD, Lee A: Mammary fibroblasts remodel fibrillar collagen microstructure in a biomimetic nanocomposite hydrogel. Acta Biomater 83: 221-232, 2019. PM30414485/PMC6291359

  16. Shahi Thakuri P, Luker GD, Tavana H: Cyclical Treatment of Colorectal Tumor Spheroids Induces Resistance to MEK Inhibitors. Transl Oncol 12(3): 404-416, 2019. PM30550927/PMC6299152

  17. Zhang Z, Chen L, Humphries B, Brien R, Wicha MS, Luker KE, Luker GD, Chen YC, Yoon E: Morphology based prediction of cancer cell migration using an artificial neural network and a random decision forest Integr Biol (Camb) Epub ahead of print: doi: 10.1039/c8ib00106e, 2018.

  18. Liu C, Chiang B, Lewin -Mejia D, Luker KE, Luker GD, Lee A: Mammary fibroblasts remodel fibrillar collagen microstructure in a biomimetic nanocomposite hydrogel Acta Biomater S1742-7061: 30664-0, 2018.

  19. Roseland ME, Kazerooni EA, Bailey JE, Luker GD, Cohan RH, Davenport MS: Needs Assessment Using a Structured Prioritization Schema: An Open Letter to PACS Vendors J Am Coll Radiol S1546-1440: 30862-7, 2018.

  20. Santos-Vizcaino E, Haley H, Gonzalez-Pujana A, Orive G, Hernandez RM, Luker GD, Pedraz JL: Monitoring implantable immunoisolation devices with intrinsic fluorescence of genipin J Biophotonics Epub ahead of print: e201800170, 2018.

  21. Hoff BA, Brisset JC, Galbán S, Van Dort M, Smith DC, Reichert ZR, Jacobson JA, Luker GD, Chenevert TL, Ross BD: Multimodal imaging provides insight into targeted therapy response in metastatic prostate cancer to the bone Am J Nucl Med Mol Imaging 8(3): 189-199, 2018. PMC6056245

  22. Haley HR, Shen N, Qyli T, Buschhaus JM, Pirone M, Luker KE, Luker GD: Enhanced Bone Metastases in Skeletally Immature Mice. Tomography 4(2): 84-93, 2018. PMC6035009

  23. Schaefer JK, Choi SM, Luker GD, Chenevert TL, Ross BD, Talpaz M: Primary myelofibrosis evolving to an aplastic appearing marrow Clin Case Rep 6(7): 1393-1395, 2018. PMC6028358

  24. Buschhaus JM, Humphries B, Luker KE, Luker GD: A Caspase-3 Reporter for Fluorescence Lifetime Imaging of Single-Cell Apoptosis. Cells 7(6): 2018. PM30720785/PMC6025355

  25. Chen YC, Humphries B, Brien R, Gibbons AE, Chen YT, Qyli T, Haley HR, Pirone ME, Chiang B, Xiao A, Cheng YH, Luan Y, Zhang Z, Cong J, Luker KE, Luker GD, Yoon E: Functional Isolation of Tumor-Initiating Cells using Microfluidic-Based Migration Identifies Phosphatidylserine Decarboxylase as a Key Regulator. Sci Rep 8(1): 244, 2018. PM29321615/PMC5762897

  26. Hoff BA, Brisset JC, Galbán S, Van Dort M, Smith DC, Reichert ZR, Jacobson JA, Luker GD, Chenevert TL, Ross BD: Multimodal imaging provides insight into targeted therapy response in metastatic prostate cancer to the bone. Am J Nucl Med Mol Imaging 8(3): 189-199, 2018. PM30042870/PMC6056245

  27. Liu C, Lewin Mejia D, Chiang B, Luker KE, Luker GD: Hybrid collagen alginate hydrogel as a platform for 3D tumor spheroid invasion. Acta Biomater 0: 0, 2018. PM29879553

  28. Luo M, Shang L, Brooks MD, Jiagge E, Zhu Y, Buschhaus JM, Conley S, Fath MA, Davis A, Gheordunescu E, Wang Y, Harouaka R, Lozier A, Triner D, McDermott S, Merajver SD, Luker GD, Spitz DR, Wicha MS: Targeting Breast Cancer Stem Cell State Equilibrium through Modulation of Redox Signaling. Cell Metab 28(1): 69-86.e6, 2018. PM29972798

  29. Jordahl JH, Solorio L, Sun H, Ramcharan S, Teeple CB, Haley HR, Lee KJ, Eyster TW, Luker GD, Krebsbach PH, Lahann J: 3D Jet Writing: Functional Microtissues Based on Tessellated Scaffold Architectures. Adv Mater 30(14): e1707196, 2018. PM29484715

  30. Gibbons AE, Luker KE, Luker GD: Dual Reporter Bioluminescence Imaging with NanoLuc and Firefly Luciferase. Methods Mol Biol 1790: 41-50, 2018. PM29858782

  31. Buschhaus JM , Luker KE, Luker GD: A Facile, In Vitro 384-Well Plate System to Model Disseminated Tumor Cells in the Bone Marrow Microenvironment. Methods Mol Biol 1686: 201-213, 2018. PM29030823

  32. Buschhaus JM , Gibbons AE, Luker KE, Luker GD: Fluorescence lifetime imaging of a caspase-3 apoptosis reporter Curr Prot Cell Biol 77: 1-21, 2017. PMC5729923

  33. Thakuri PS, Liu C, Luker GD, Tavana H: Biomaterials-based approaches to tumor spheroid and organoid modeling Adv Healthc Mat doi: 10.1002/adhm.201700980: doi: 10.1002/adhm.201700980, 2017.

  34. Lesher-Pérez SC, Kim GA, Kuo CH, Leung BM, Mong S, Kojima T, Moraes C, Thouless MD, Luker GD, Takayama S: Dispersible oxygen microsensors map oxygen gradients in three-dimensional cell cultures. Biomater Sci 5(10): 2106-2113, 2017. PM28805850/PMC5678941

  35. Van Dort ME, Galbán S, Nino CA, Hong H, Apfelbaum AA, Luker GD, Thurber GM, Atangcho L, Besirli CG, Ross BD: Structure-Guided Design and Initial Studies of a Bifunctional MEK/PI3K Inhibitor (ST-168). ACS Med Chem Lett 8(8): 808-813, 2017. PM28835793/PMC5554897

  36. Chang SL, Cavnar SP, Luker KE, Takayama S, Luker GD, Linderman JJ: Correction: Cell, Isoform, and Environment Factors Shape Gradients and Modulate Chemotaxis. PLoS One 12(3): e0174189, 2017. PM28291822

  37. Spinosa PC, Luker KE, Luker GD, Linderman JJ: The CXCL12/CXCR7 signaling axis, isoforms, circadian rhythms, and tumor cellular composition dictate gradients in tissue. PLoS One 12(11): e0187357, 2017. PM29117251/PMC5678865

  38. Ham SL, Thakuri PS, Plaster M, Li J, Luker KE, Luker GD, Tavana H: Three-dimensional tumor model mimics stromal - breast cancer cells signaling. Oncotarget 9(1): 249-267, 2017. PM29416611/PMC5787462

  39. Galbán S, Apfelbaum AA, Espinoza C, Heist K, Haley H, Bedi K, Ljungman M, Galbán CJ, Luker GD, Dort MV, Ross BD: A Bifunctional MAPK/PI3K Antagonist for Inhibition of Tumor Growth and Metastasis. Mol Cancer Ther 16(11): 2340-2350, 2017. PM28775144/PMC5669819

  40. Rajasekaran D, Gröning S, Schmitz C, Zierow S, Drucker N, Bakou M, Kohl K, Mertens A, Lue H, Weber C, Xiao A, Luker G, Kapurniotu A, Lolis E, Bernhagen J: Macrophage migration inhibitory factor-CXCR4 receptor interactions: Evidence for partial allosteric agonism in comparison with CXCL12 chemokine Journal of Biological Chemistry 291(30): 15881-15895, 2016. PM27226569

  41. Shahi Thakuri P, Ham SL, Luker GD, Tavana H: Multiparametric Analysis of Oncology Drug Screening with Aqueous Two-Phase Tumor Spheroids. Mol Pharm 13(11): 3724-3735, 2016. PM27653969

  42. Luker GD, Nguyen HM, Hoff BA, Galbán CJ, Hernando D, Chenevert TL, Talpaz M, Ross BD: A Pilot Study of Quantitative MRI Parametric Response Mapping of Bone Marrow Fat for Treatment Assessment in Myelofibrosis. Tomography 2(1): 67-78, 2016. PM27213182/PMC4872873

  43. Ham SL, Joshi R, Luker GD, Tavana H: Engineered Breast Cancer Cell Spheroids Reproduce Biologic Properties of Solid Tumors. Adv Healthc Mater 5(21): 2788-2798, 2016. PM27603912/PMC5142748

  44. Keith L, Ross BD, Galbán CJ, Luker GD, Galbán S, Zhao B, Guo X, Chenevert TL, Hoff BA: Semiautomated Workflow for Clinically Streamlined Glioma Parametric Response Mapping. Tomography 2(4): 267-275, 2016. PM28286871/PMC5345939

  45. Cavnar SP, Xiao A, Gibbons AE, Rickelmann AD, Neely T, Luker KE, Takayama S, Luker GD: Imaging Sensitivity of Quiescent Cancer Cells to Metabolic Perturbations in Bone Marrow Spheroids. Tomography 2(2): 146-157, 2016. PM27478871/PMC4963031

  46. Yang D, Feng L, Dougherty CA, Luker KE, Chen D, Cauble MA, Banaszak Holl MM, Luker GD, Ross BD, Liu Z, Hong H: In vivo targeting of metastatic breast cancer via tumor vasculature-specific nano-graphene oxide. Biomaterials 104: 361-71, 2016. PM27490486

  47. Rajasekaran D, Gröning S, Schmitz C, Zierow S, Drucker N, Bakou M, Kohl K, Mertens A, Lue H, Weber C, Xiao A, Luker G, Kapurniotu A, Lolis EJ, Bernhagen J.: Macrophage Migration Inhibitory Factor-CXCR4 Receptor Interactions: Evidence for Partial Allosteric Agonism in Comparison to CXCL12 J Biol Chem May 19. pii: jbc.M116.717751.: [Epub ahead of print], 2016. PMID: 27226569

  48. Luker GD, Nguyen HM, Hoff BA, Galban CJ, Hernando D, Chenevert TL, Talpaz M, Ross BD: A Pilot Study of Quantitative MRI Parametric Response Mapping of Bone Marrow Fat for Treatment Assessment in Myelofibrosis Tomography 2(1): 67-78, 2016. PMC4872873

  49. Luker KE, Luker GD: Dual-Color Luciferase Complementation for Chemokine Receptor Signaling. Methods Enzymol 570: 119-29, 2016. PM26921944

  50. Behnam Azad B, Lisok A, Chatterjee S, Poirier JT, Pullambhatla M, Luker GD, Pomper MG, Nimmagadda S: Targeted Imaging of the Atypical Chemokine Receptor 3 (ACKR3/CXCR7) in Human Cancer Xenografts. J Nucl Med Feb 23. pii: jnumed.115.167932: [Epub ahead of print], 2016. PM26912435

  51. Xiang J, Hurchla MA, Fontana F, Su X, Amend SR, Esser AK, Douglas GJ, Mudalagiriyappa C, Luker KE, Pluard T, Ademuyiwa FO, Romagnoli B, Tuffin G, Chevalier E, Luker GD, Bauer M, Zimmermann J, Aft RL, Dembowsky K, Weilbaecher KN: CXCR4 Protein Epitope Mimetic Antagonist, POL5551, Disrupts Metastasis and Enhances Chemotherapy Effect in Triple Negative Breast Cancer. Molecular cancer therapeutics 11: 2473-2485, 2015. PM26269605

  52. Misra AC, Luker KE, Durmaz H, Luker GD, Lahann J: CXCR4-Targeted Nanocarriers for Triple Negative Breast Cancers. Biomacromolecules 16(8): 2412-7, 2015. PM26154069

  53. Stacer AC , Fenner J, Cavnar SP, Xiao A, Zhao S, Chang SL, Salomonnson A, Luker KE, Luker GD: Endothelial CXCR7 regulates breast cancer metastasis. Oncogene 35(13): 1716-1724, 2015. PM26119946/PMC4486335

  54. Stacer AC , Wang H, Fenner J, Dosch JS, Salomonnson A, Luker KE, Luker GD, Rehemtulla A, Ross BD: Imaging Reporters for Proteasome Activity Identify Tumor- and Metastasis-Initiating Cells. Mol Imaging 14(8): 414-432, 2015. PM28654354

  55. Xiao A, Gibbons AE, Luker KE, Luker GD: Fluorescence Lifetime Imaging of Apoptosis. Tomography 1(2): 115-124, 2015. PM26771007/PMC4710058

  56. Hoff BA, Toole M, Yablon C, Ross BD, Luker GD, VanPoznak C, Galbán CJ: Potential for Early Fracture Risk Assessment in Patients with Metastatic Bone Disease using Parametric Response Mapping of CT Images. Tomography 1(2): 98-104, 2015. PM26771006/PMC4710140

  57. Ham SL, Nasrollahi S, Shah KN, Soltisz A, Paruchuri S, Yun YH, Luker GD, Bishayee A, Tavana H: Phytochemicals potently inhibit migration of metastatic breast cancer cells. Integr Biol (Camb) 7(7): 792-800, 2015. PM26120051

  58. Cavnar SP , Rickelmann AD, Meguiar KF, Xiao A, Dosch J, Leung BM, Cai Lesher-Perez S, Chitta S, Luker KE, Takayama S, Luker GD: Modeling Selective Elimination of Quiescent Cancer Cells from Bone Marrow. Neoplasia 17(8): 625-33, 2015. PM26408255

  59. Stacer AC (*trainee), Wang H, Fenner J, Dosch JS, Salomonnson A, Luker KE, Luker GD, Rehemtulla A, Ross BD: Imaging Reporters for Proteasome Activity Identify Tumor- and Metastasis-Initiating Cells. Mol Imaging 14: 414-28, 2015. PM26431589

  60. Luker KE, Pata P, Shemiakina II, Pereverzeva A, Stacer AC, Shcherbo DS, Pletnev VZ, Skolnaja M, Lukyanov KA, Luker GD, Pata I, Chudakov DM: Comparative study reveals better far-red fluorescent protein for whole body imaging. Scientific reports 5: 10332, 2015. PM26035795

  61. Stacer AC (*trainee) , Fenner J, Cavnar SP, Xiao A, Zhao S, Chang SL, Salomonnson A, Luker KE, Luker, GD: Endothelial CXCR7 Regulates Breast Cancer Metastasis Oncogene 2015: in press, 2015.

  62. Chang SL, Cavnar SP, Takayama S, Luker GD, Linderman JJ: Cell, isoform, and environment factors shape gradients and modulate chemotaxis. PloS one 10(4): e0123450, 2015. PM25909600

  63. Kojima T, Moraes C, Cavnar SP, Luker GD, Takayama S: Surface-templated hydrogel patterns prompt matrix-dependent migration of breast cancer cells towards chemokine-secreting cells. Acta biomaterialia 13: 68-77, 2015. PM25463502

  64. Coggins NL (*trainee), Trakimas D, Chang SL, Ehrlich A, Ray P, Luker KE, Linderman JJ, Luker GD: CXCR7 controls competition for recruitment of β-arrestin 2 in cells expressing both CXCR4 and CXCR7 PLoS One 9(6): e98328, 2014.

  65. Ray P (*trainee), Stacer AC, Fenner J, Cavnar SP, Meguiar K, Brown M, Luker KE, Luker GD: CXCL12-γ in primary tumors drives breast cancer metastasis Oncogene 9: 157, 2014.

  66. Cavnar SP (*trainee), Ray P, Moudgil P, Chang SL, Luker KE, Linderman JJ, Takayama S, Luker GD : Microfluidic source-sink model reveals effects of biophysically distinct CXCL12 isoforms in breast cancer chemotaxis Integr Biol (Camb) 6: 564-576, 2014.

  67. Cavnar SP (*trainee), Ray P, Moudgil P, Chang SL, Luker KE, Linderman JJ, Takayama S, Luker GD: Microfluidic source-sink model reveals effects of biophysically distinct CXCL12 isoforms in breast cancer chemotaxis. Integrative biology : quantitative biosciences from nano to macro 6(5): 564-76, 2014. PM24675873

  68. Cavnar SP (*trainee), Salomonsson E, Luker KE, Luker GD, Takayama S: Transfer, imaging, and analysis plate for facile handling of 384 hanging drop 3D tissue spheroids. Journal of laboratory automation 19(2): 208-14, 2014. PM24051516

  69. Zhang Z, Shiratsuchi H, Lin J, Chen G, Reddy RM, Azizi E, Fouladdel S, Chang AC, Lin L, Jiang H, Waghray M, Luker G, Simeone DM, Wicha MS, Beer DG, Ramnath N, Nagrath S: Expansion of CTCs from early stage lung cancer patients using a microfluidic co-culture model Oncotarget 5(23): 12383-12397, 2014. PM25474037

  70. Coggins NL, Trakimas D, Chang SL, Ehrlich A, Ray P, Luker KE, Linderman JJ, Luker GD: CXCR7 controls competition for recruitment of β-arrestin 2 in cells expressing both CXCR4 and CXCR7. PloS one 9(6): e98328, 2014. PM24896823

  71. Zhao S, Chang SL, Linderman JJ, Feng FY, Luker GD: A Comprehensive Analysis of CXCL12 Isoforms in Breast Cancer1,2. Translational oncology 0: 0, 2014. PM24836649

  72. Ray P, Stacer AC, Fenner J, Cavnar SP, Meguiar K, Brown M, Luker KE, Luker GD: CXCL12-γ in primary tumors drives breast cancer metastasis. Oncogene 34(16): 2043-2051, 2014. PM24909174

  73. Fenner J, Stacer AC, Winterroth F, Johnson TD, Luker KE, Luker GD: Macroscopic stiffness of breast tumors predicts metastasis. Scientific reports 4: 5512, 2014. PM24981707

  74. Lemmo S, Atefi E, Luker GD, Tavana H: Optimization of Aqueous Biphasic Tumor Spheroid Microtechnology for Anti-Cancer Drug Testing in 3D Culture. Cellular and molecular bioengineering 7(3): 344-354, 2014. PM25221631

  75. Atefi E, Lemmo S, Fyffe D, Luker GD, Tavana H: High Throughput, Polymeric Aqueous Two-Phase Printing of Tumor Spheroids. Advanced functional materials 24(41): 6509-6515, 2014. PM25411577

  76. Leung BM, Moraes C, Cavnar SP, Luker KE, Luker GD, Takayama S: Microscale 3D Collagen Cell Culture Assays in Conventional Flat-Bottom 384-Well Plates. Journal of laboratory automation 2: 138-145, 2014. PM25510473

  77. Luker KE, Luker GD: Split Gaussia luciferase for imaging ligand-receptor binding Methods Mol. Biol. 1098: 59-69, 2014. PM24166368

  78. Ehrlich A, Ray P, Luker KE, Lolis EJ, Luker GD: Allosteric peptide regulators of chemokine receptors CXCR4 and CXCR7 Biochem. Pharmacol. 86(9): 1263-1271, 2013. PM23973527

  79. Stacer AC (*trainee) , Nyati S, Moudgil P, Iyengar R, Luker KE, Rehemtulla A, Luker GD: NanoLuc reporter for dual luciferase imaging in living animals. Mol Imaging 12(7): 1-13, 2013. PM24371848

  80. Toubai T, Sun Y, Luker G, Liu J, Luker KE, Tawara I, Evers R, Liu C, Mathewson N, Malter C, Nieves E, Choi S, Murphy KM, Reddy P: Host-derived CD8+ dendritic cells are required for induction of optimal graftversus- tumor responses after experimental allogeneic bone marrow transplantation. Blood 121(20): 4231- 4241, 2013. PM23520337

  81. Lai D, Labuz JM, Kim J, Luker GD, Shikanov A, Takayama S: Simple Multi-level Microchannel Fabrication by Pseudo-Grayscale Backside Diffused Light Lithography. RSC advances 3(42): 19467-19473, 2013. PM24976950

  82. Salomonnson E (*trainee), Stacer AC, Ehrlich A, Luker KE, Luker GD: Imaging CXCL12-CXCR4 signaling in ovarian cancer therapy. PLoS ONE 8(1): e51500, 2013. PM23372646

  83. Sevick-Muraca EM, Akers WJ, Joshi BP, Luker GD, Cutler CS, Marnett LJ, Contag CH, Wang TD, Azhdarinia A: Advancing the translation of optical imaging agents for clinical imaging. Biomed Opt Express 4(1): 160-170, 2013. PM23304655

  84. Mehta G, Hsiao AY, Ingram M, Luker GD, Takayama S: Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy. J Control Release 164(2): 192-204, 2012. PM22613880

  85. Luker KE, Lewin SA, Mihalko LA, Schmidt BT, Winkler JS, Coggins NL, Thomas DG, Luker GD: Scavenging of CXCL12 by CXCR7 promotes tumor growth and metastasis of CXCR4-positive breast cancer cells. Oncogene 31(45): 4750-4758, 2012. PM22266857

  86. Fang Y, Frampton JP, Raghavan S, Sabahi-Kaviani R, Luker G, Deng CX, Takayama S: Rapid generation of multiplexed cell cocultures using acoustic droplet ejection followed by aqueous two-phase exclusion patterning. Tissue Eng Part C Methods 18(9): 647-657, 2012. PM22356298

  87. Ray P (*trainee) , Mihalko LA, Coggins NL, Moudgil P, Ehrlich A, Luker KE, Luker GD: Carboxy-terminus of CXCR7 regulates receptor localization and function. Int. J. Biochem. Cell Biol. 44(4): 669-678, 2012. PM22300987

  88. Ray P (*trainee), Lewin SA, Mihalko LA, Lesher-Perez SC, Takayama S, Luker KE, Luker GD: Secreted CXCL12 (SDF-1) forms dimers under physiological conditions. Biochem. J. 442(2): 433-442, 2012. PM22142194

  89. Luker KE, Mihalko LA, Schmidt BT, Lewin SA, Ray P, Shcherbo D, Chudakov DM, Luker GD: In vivo imaging of ligand receptor binding with Gaussia luciferase complementation Nat. Med. 18(1): 172-177, 2012. PM22138753

  90. Salomonnson E (*trainee) , Mihalko LA, Verkhusha VV, Luker KE, Luker GD: Cell-based and in vivo spectral analysis of fluorescent proteins for multiphoton microscopy. J Biomed Opt 17(9): 96001, 2012. PM22975677

  91. Bunschoten A, Buckle T, Kuil J, Luker GD, Luker KE, Nieweg OE, van Leeuwen FW: Targeted noncovalent self-assembled nanoparticles based on human serum albumin. Biomaterials 33(3): 867-875, 2012. PM22024362

  92. Ray P (*trainee) , Lewin SA, Mihalko LA, Schmidt BT, Luker KE, Luker GD: Noninvasive imaging reveals inhibition of ovarian cancer by targeting CXCL12-CXCR4 Neoplasia 13(12): 1152-1161, 2011. PM22241961

  93. Elahi SF, Liu Z, Luker KE, Kwon RS, Luker GD, Wang TD: Longitudinal Molecular Imaging with Single Cell Resolution of Disseminated Ovarian Cancer in Mice with a LED-based Confocal Microendoscope. Mol Imaging Biol 13(6): 1157-1162, 2011. PM21136184

  94. Tavana H, Kaylan K, Bersano-Begey T, Luker KE, Luker GD, Takayama S: Polymeric Aqueous Biphasic System Rehydration Facilitates High Throughput Cell Exclusion Patterning For Cell Migration Studies. Advanced functional materials 21(15): 2920-2926, 2011. PM23519702

  95. Cruz-Orengo L, Holman DW, Dorsey D, Zhou L, Zhang P, Wright M, McCandless EE, Patel JR, Luker GD, Littman DR, Russell JH, Klein RS: CXCR7 influences leukocyte entry into the CNS parenchyma by controlling abluminal CXCL12 abundance during autoimmunity. J. Exp. Med. 208(2): 327-339, 2011. PM21300915

  96. Bhattacharya D, Bensaci M, Luker KE, Luker G, Wisdom S, Telford SR, Hu LT: Development of a baited oral vaccine for use in reservoir-targeted strategies against Lyme disease. Vaccine 29(44): 7818-7825, 2011. PM21816190

  97. Bhojani MS, Ranga R, Luker GD, Rehemtulla A, Ross BD, Van Dort ME: Synthesis and Investigation of a Radioiodinated F3 Peptide Analog as a SPECT Tumor Imaging Radioligand. PLoS ONE 6(7): e22418. 2011. PM21811604

  98. Luker GD, Luker KE: Luciferase protein complementation assays for bioluminescence imaging of cells and mice. Methods Mol. Biol. 680: 29-43, 2011. PM21153371

  99. Huang NT, Truxal SC, Tung YC, Hsiao AY, Luker GD, Takayama S, Kurabayashi K: Multiplexed spectral signature detection for microfluidic color-coded bioparticle flow. Anal. Chem. 82(22): 9506-9512, 2010. PM20979407

  100. Torisawa YS, Mosadegh B, Bersano-Begey T, Steele JM, Luker KE, Luker GD, Takayama S: Microfluidic platform for chemotaxis in gradients formed by CXCL12 source-sink cells. Integr Biol (Camb) 2(11-12): 680-686, 2010. PM20871938/PMC-

  101. Shcherbo D, Shemiakina II, Ryabova AV, Luker KE, Schmidt BT, Souslova EA, Gorodnicheva TV, Strukova L, Shidlovskiy KM, Britanova OV, Zaraisky AG, Lukyanov KA, Loschenov VB, Luker GD, Chudakov DM: Near-infrared fluorescent proteins. Nat. Methods 7(10): 827-829, 2010. PM20818379

  102. Luker KE, Steele JM, Mihalko LA, Ray P, Luker GD: Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene 29 (32): 4599-4610, 2010. PM20531309

  103. Luker KE, Luker GD: Bioluminescence imaging of reporter mice for studies of infection and inflammation. Antiviral Res. 86(1): 93-100, 2010. PM20417377/PMC2863000

  104. Torisawa YS, Mosadegh B, Luker GD, Morell M, O'Shea KS, Takayama S: Microfluidic hydrodynamic cellular patterning for systematic formation of co-culture spheroids. Integr Biol (Camb) 1(11-12): 649-654, 2009. PM20027373/PMC2825702

  105. Luker KE, Gupta M, Steele JM, Foerster BR, Luker GD: Imaging ligand-dependent activation of CXCR7. Neoplasia 11(10): 1022-1035, 2009. PM19794961/PMC2745668

  106. Tavana H, Jovic A, Mosadegh B, Lee QY, Liu X, Luker KE, Luker GD, Weiss SJ, Takayama S: Nanolitre liquid patterning in aqueous environments for spatially defined reagent delivery to mammalian cells. Nat Mater 8(9): 736-741, 2009. PM19684584/PMC2782768

  107. Luker K, Gupta M, Luker G: Bioluminescent CXCL12 fusion protein for cellular studies of CXCR4 and CXCR7. BioTechniques 47(1): 625-632, 2009. PM19594447/PMC-

  108. Luker KE, Gupta M, Luker GD: Imaging chemokine receptor dimerization with firefly luciferase complementation. FASEB J. 23(3): 823-834, 2009. PM19001056/PMC2653984

  109. Luker KE, Luker GD: Real-time bioluminescence imaging of viral pathogenesis. Methods Mol. Biol. 574: 125-135, 2009. PM19685305/PMC-

  110. Song JW, Cavnar SP, Walker AC, Luker KE, Gupta M, Tung YC, Luker GD, Takayama S: Microfluidic endothelium for studying the intravascular adhesion of metastatic breast cancer cells. PLoS ONE 4(6): e5756, 2009. PM19484126/PMC2684591

  111. Pichler A, Prior JL, Luker GD, Piwnica-Worms D: Generation of a highly inducible Gal4-->Fluc universal reporter mouse for in vivo bioluminescence imaging. Proc. Natl. Acad. Sci. U.S.A. 105(41): 15932-15937, 2008. PM18843112/PMC2572923

  112. Tkaczyk ER, Tkaczyk AH, Katnik S, Ye JY, Luker KE, Luker GD, Myc A, Baker JR, Norris TB: Extended cavity laser enhanced two-photon flow cytometry. J Biomed Opt 13(4): 041319, 2008. PM19021327/PMC-

  113. Eliane JP, Repollet M, Luker KE, Brown M, Rae JM, Dontu G, Schott AF, Wicha M, Doyle GV, Hayes DF, Luker GD: Monitoring serial changes in circulating human breast cancer cells in murine xenograft models. Cancer Res. 68(14): 5529-5532, 2008. PM18632603/PMC2789403

  114. Luker KE, Gupta M, Luker GD: Imaging CXCR4 signaling with firefly luciferase complementation. Anal. Chem. 80(14): 5565-5573, 2008. PM18533683/PMC-

  115. Luker KE, Luker GD: Applications of bioluminescence imaging to antiviral research and therapy: multiple luciferase enzymes and quantitation. Antiviral Res. 78(3): 179-187, 2008. PM18358543/PMC2430099

  116. Tkaczyk ER, Zhong CF, Ye JY, Myc A, Thomas T, Cao Z, Duran-Struuck R, Luker KE, Luker GD, Norris TB, Baker JR: In Vivo Monitoring of Multiple Circulating Cell Populations Using Two-photon Flow Cytometry. Optics communications 281(4): 888-894, 2008. PM19221581

  117. Bielinska AU, Chepurnov AA, Landers JJ, Janczak KW, Chepurnova TS, Luker GD, Baker JR: A novel, killed-virus nasal vaccinia virus vaccine. Clin. Vaccine Immunol. 15(2): 348-358, 2008. PM18057181/PMC2238057

  118. Hutchens MA (*trainee) , Luker KE, Sonstein J, Núñez G, Curtis JL, Luker GD: Protective effect of Tolllike receptor 4 in pulmonary vaccinia infection. PLoS Pathog. 4(9): e1000153, 2008. PM18802464/PMC2529451

  119. Hutchens M (*trainee), Luker KE, Sottile P, Sonstein J, Lukacs NW, Núñez G, Curtis JL, Luker GD: TLR3 increases disease morbidity and mortality from vaccinia infection. J. Immunol. 180(1): 483-491, 2008. PM18097050/PMC-

  120. Luker GD, Luker KE: Optical imaging: current applications and future directions. J. Nucl. Med. 49(1): 1-4, 2008. PM18077528/PMC-

  121. Rudd BD, Luker GD, Luker KE, Peebles RS, Lukacs NW: Type I interferon regulates respiratory virus infected dendritic cell maturation and cytokine production. Viral Immunol. 20(4): 531-540, 2007. PM18158727

  122. Duran-Struuck R, Tawara I, Lowler K, Clouthier SG, Weisiger E, Rogers C, Luker G, Kumanogoh A, Liu C, Ferrara JL, Reddy P: A novel role for the semaphorin Sema4D in the induction of allo-responses. Biol. Blood Marrow Transplant. 13(11): 1294-1303.e1, 2007. PM17950916

  123. Miao Z, Luker KE, Summers BC, Berahovich R, Bhojani MS, Rehemtulla A, Kleer CG, Essner JJ, Nasevicius A, Luker GD, Howard MC, Schall TJ: CXCR7 (RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature. Proc. Natl. Acad. Sci. U.S.A. 104(40): 15735-15740, 2007. PM17898181

  124. Hutchens M (*trainee), Luker GD: Applications of bioluminescence imaging to the study of infectious diseases. Cell. Microbiol. 9(10): 2315-2322, 2007. PM17587328

  125. Rivera R (*trainee) , Hutchens M, Luker KE, Sonstein J, Curtis JL, Luker GD: Murine alveolar macrophages limit replication of vaccinia virus Virology 363(1): 48-58, 2007. PM17331554

  126. Yao Y, Li P, Singh P, Thiele AT, Wilkes DS, Renukaradhya GJ, Brutkiewicz RR, Travers JB, Luker GD, Hong SC, Blum JS, Chang CH: Vaccinia virus infection induces dendritic cell maturation but inhibits antigen presentation by MHC class II. Cell. Immunol. 246(2): 92-102, 2007. PM17678637

  127. Luker KE, Schultz T, Romine J, Leib DA, Luker GD: Transgenic reporter mouse for bioluminescence imaging of herpes simplex virus 1 infection in living mice. Virology 347(2): 286-295, 2006. PM16430938

  128. Luker KE, Luker GD: Functions of CXCL12 and CXCR4 in breast cancer. Cancer Lett. 238(1): 30-41, 2006. PM16046252

  129. Luker KE, Hutchens M, Schultz T, Pekosz A, Luker GD: Bioluminescence imaging of vaccinia virus: effects of interferon on viral replication and spread. Virology 341(2): 284-300, 2005. PM16095645

  130. Luker GD, Leib DA: Luciferase real-time bioluminescence imaging for the study of viral pathogenesis. Methods Mol. Biol. 292: 285-296, 2005. PM15507716

  131. Smith MC, Luker KE, Garbow JR, Prior JL, Jackson E, Piwnica-Worms D, Luker GD: CXCR4 regulates growth of both primary and metastatic breast cancer. Cancer Res. 64(23): 8604-8612, 2004. PM15574767

  132. Luker KE, Smith MC, Luker GD, Gammon ST, Piwnica-Worms H, Piwnica-Worms D: Kinetics of regulated protein-protein interactions revealed with firefly luciferase complementation imaging in cells and living animals. Proc. Natl. Acad. Sci. U.S.A. 101(33): 12288-12293, 2004. PM15284440

  133. Barreiro R, Luker G, Herndon J, Ferguson TA: Termination of antigen-specific immunity by CD95 ligand (Fas ligand) and IL-10. J. Immunol. 173(3): 1519-1525, 2004. PM15265879

  134. Krug A, Luker GD, Barchet W, Leib DA, Akira S, Colonna M: Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 103(4): 1433-1437, 2004. PM14563635

  135. Luker GD, Prior JL, Song J, Pica CM, Leib DA: Bioluminescence imaging reveals systemic dissemination of herpes simplex virus type 1 in the absence of interferon receptors. J. Virol. 77(20): 11082-11093, 2003. PM14512556

  136. Luker GD, Pica CM, Song J, Luker KE, Piwnica-Worms D: Imaging 26S proteasome activity and inhibition in living mice. Nat. Med. 9(7): 969-973, 2003. PM12819780

  137. Richard JC, Zhou Z, Ponde DE, Dence CS, Factor P, Reynolds PN, Luker GD, Sharma V, Ferkol T, Piwnica-Worms D, Schuster DP: Imaging pulmonary gene expression with positron emission tomography. Am. J. Respir. Crit. Care Med. 167(9): 1257-1263, 2003. PM12505860

  138. Luker GD, Sharma V, Pica CM, Prior JL, Li W, Piwnica-Worms D: Molecular imaging of protein-protein interactions: controlled expression of p53 and large T-antigen fusion proteins in vivo. Cancer Res. 63(8): 1780-1788, 2003. PM12702563

  139. Luker GD, Sharma V, Piwnica-Worms D: Visualizing protein-protein interactions in living animals. Methods 29(1): 110-122, 2003. PM12543076

  140. Luker GD, Bardill JP, Prior JL, Pica CM, Piwnica-Worms D, Leib DA: Noninvasive bioluminescence imaging of herpes simplex virus type 1 infection and therapy in living mice. J. Virol. 76(23): 12149-12161, 2002. PM12414955

  141. Luker GD, Sharma V, Pica CM, Dahlheimer JL, Li W, Ochesky J, Ryan CE, Piwnica-Worms H, Piwnica-Worms D: Noninvasive imaging of protein-protein interactions in living animals. Proc. Natl. Acad. Sci. U.S.A. 99(10): 6961-6966, 2002. PM11997447

  142. Luker GD, Luker KE, Sharma V, Pica CM, Dahlheimer JL, Ocheskey JA, Fahrner TJ, Milbrandt J, Piwnica-Worms D: In vitro and in vivo characterization of a dual-function green fluorescent protein--HSV1-thymidine kinase reporter gene driven by the human elongation factor 1 alpha promoter. Mol Imaging 1(2): 65-73, 2002. PM12920846

  143. Sharma V, Luker GD, Piwnica-Worms D: Molecular imaging of gene expression and protein function in vivo with PET and SPECT. J Magn Reson Imaging 16(4): 336-351, 2002. PM12353250

  144. Luker GD: Special conference of the American Association for Cancer Research on molecular imaging in cancer: linking biology, function, and clinical applications in vivo. Cancer Res. 62(7): 2195-2198, 2002. PM11929844

  145. Luker GD, Flagg TP, Sha Q, Luker KE, Pica CM, Nichols CG, Piwnica-Worms D: MDR1 P-glycoprotein reduces influx of substrates without affecting membrane potential. J. Biol. Chem. 276(52): 49053-49060, 2001. PM11598111

  146. Luker GD, Dahlheimer JL, Ostlund RE, Piwnica-Worms D: Decreased hepatic accumulation and enhanced esterification of cholesterol in mice deficient in mdr1a and mdr1b P-glycoproteins. J. Lipid Res. 42(9): 1389-1394, 2001. PM11518757

  147. Luker GD, Piwnica-Worms D: Molecular imaging in vivo with PET and SPECT. Acad Radiol 8(1): 4-14, 2001. PM11201455

  148. Polyakov V, Sharma V, Dahlheimer JL, Pica CM, Luker GD, Piwnica-Worms D: Novel Tat-peptide chelates for direct transduction of technetium-99m and rhenium into human cells for imaging and radiotherapy. Bioconjug. Chem. 11(6): 762-771, 2000. PM11087323

  149. Chen WS, Luker KE, Dahlheimer JL, Pica CM, Luker GD, Piwnica-Worms D: Effects of MDR1 and MDR3 P-glycoproteins, MRP1, and BCRP/MXR/ABCP on the transport of (99m)Tc-tetrofosmin. Biochem. Pharmacol. 60(3): 413-426, 2000. PM10856437

  150. Luker GD, Pica CM, Kumar AS, Covey DF, Piwnica-Worms D: Effects of cholesterol and enantiomeric cholesterol on P-glycoprotein localization and function in low-density membrane domains. Biochemistry 39 (26): 7651-7661, 2000. PM10869171

  151. Luker GD, Pica CM, Kumar AS, Covey DF, Piwnica-Worms D: Effects of cholesterol and enantiomeric cholesterol on P-glycoprotein localization and function in low-density membrane domains Biochemistry 39 (29): 8692, 2000. PM10913278

  152. Luker GD, Nilsson KR, Covey DF, Piwnica-Worms D: Multidrug resistance (MDR1) P-glycoprotein enhances esterification of plasma membrane cholesterol. J. Biol. Chem. 274(11): 6979-6991, 1999. PM10066752

  153. Kronemer KA, Don S, Luker GD, Hildebolt C: Soft-copy versus hard-copy interpretation of voiding cystourethrography in neonates, infants, and children. AJR Am J Roentgenol 172(3): 791-793, 1999. PM10063884

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