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Wei Zheng, … , Aleksanteri Aspelund, Kari Alitalo
Published March 3, 2014
Citation Information: J Clin Invest. 2014;124(3):878-887. https://doi.org/10.1172/JCI71603.
Citation Information: J Clin Invest. 2014;124(3):878-887. https://doi.org/10.1172/JCI71603.
Abstract
Lymphangiogenesis, the growth of lymphatic vessels, is essential in embryonic development. In adults, it is involved in many pathological processes such as lymphedema, inflammatory diseases, and tumor metastasis. Advances during the past decade have dramatically increased the knowledge of the mechanisms of lymphangiogenesis, including the roles of transcription factors, lymphangiogenic growth factors and their receptors, and intercellular and intracellular signaling cascades. Strategies based on these mechanisms are being tested in the treatment of various human diseases such as cancer, lymphedema, and tissue allograft rejection. This Review summarizes the recent progress on lymphangiogenic mechanisms and their applications in disease treatment.
Authors
Wei Zheng, Aleksanteri Aspelund, Kari Alitalo
Total citations by year
Citation information
Citations to this article (178)
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Multipotent Adult Progenitor Cells Support Lymphatic Regeneration at Multiple Anatomical Levels during Wound Healing and Lymphedema
M Beerens, XL Aranguren, B Hendrickx, W Dheedene, T Dresselaers, U Himmelreich, C Verfaillie, A Luttun |
Scientific Reports | 2018 |
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The chromosome 11q13.3 amplification associated lymph node metastasis is driven by miR-548k through modulating tumor microenvironment
W Zhang, R Hong, L Li, Y Wang, P Du, Y Ou, Z Zhao, X Liu, W Xiao, D Dong, Q Wu, J Chen, Y Song, Q Zhan |
Molecular Cancer | 2018 |
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uPARAP/Endo180 receptor is a gatekeeper of VEGFR-2/VEGFR-3 heterodimerisation during pathological lymphangiogenesis
T Durré, F Morfoisse, C Erpicum, M Ebroin, S Blacher, M García-Caballero, C Deroanne, T Louis, C Balsat, MV de Velde, S Kaijalainen, F Kridelka, L Engelholm, I Struman, K Alitalo, N Behrendt, J Paupert, A Noel |
Nature Communications | 2018 |
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Counterbalance: modulation of VEGF/VEGFR activities by TNFSF15
GL Yang, LY Li |
Signal Transduction and Targeted Therapy | 2018 |
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The Intestinal Lymphatic System: Functions and Metabolic Implications
V Cifarelli, A Eichmann |
CMGH Cellular and Molecular Gastroenterology and Hepatology | 2018 |
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Roles of the TGF-β–VEGF-C Pathway in Fibrosis-Related Lymphangiogenesis
H Kinashi, Y Ito, T Sun, T Katsuno, Y Takei |
International journal of molecular sciences | 2018 |
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Impact of Lymphangiogenesis on Cardiac Remodeling After Ischemia and Reperfusion Injury
Y Shimizu, R Polavarapu, KL Eskla, Y Pantner, CK Nicholson, M Ishii, D Brunnhoelzl, R Mauria, A Husain, N Naqvi, T Murohara, JW Calvert |
Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease | 2018 |
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Beneficial effects of sunitinib on tumor microenvironment and immunotherapy targeting death receptor5
Y Tsukita, T Okazaki, S Ebihara, R Komatsu, M Nihei, M Kobayashi, T Hirano, H Sugiura, T Tamada, N Tanaka, Y Sato, H Yagita, M Ichinose |
OncoImmunology | 2018 |
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Matrix stiffness controls lymphatic vessel formation through regulation of a GATA2-dependent transcriptional program
M Frye, A Taddei, C Dierkes, I Martinez-Corral, M Fielden, H Ortsäter, J Kazenwadel, DP Calado, P Ostergaard, M Salminen, L He, NL Harvey, F Kiefer, T Mäkinen |
Nature Communications | 2018 |
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Lymphatic Tissue Engineering and Regeneration
L Alderfer, A Wei, D Hanjaya-Putra |
Journal of biological engineering | 2018 |
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Targeting lymphatic function as a novel therapeutic intervention for rheumatoid arthritis
EM Bouta, RD Bell, H Rahimi, L Xing, RW Wood, CO Bingham, CT Ritchlin, EM Schwarz |
Nature Reviews Rheumatology | 2018 |
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VEGF-C promotes the development of lymphatics in bone and bone loss
D Hominick, A Silva, N Khurana, Y Liu, PC Dechow, JQ Feng, B Pytowski, JM Rutkowski, K Alitalo, MT Dellinger |
eLife | 2018 |
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Growth and Immune Evasion of Lymph Node Metastasis
D Jones, ER Pereira, TP Padera |
Frontiers in Oncology | 2018 |
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Endothelial Metabolic Control of Lymphangiogenesis
P Yu, G Wu, HW Lee, M Simons |
BioEssays : news and reviews in molecular, cellular and developmental biology | 2018 |
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Lymphatics-associated genes are downregulated at transcription level in non-small cell lung cancer
O Kowalczuk, J Laudanski, W Laudanski, W Niklinska, M Kozlowski, J Niklinski |
Oncology Letters | 2018 |
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AutoTube: a novel software for the automated morphometric analysis of vascular networks in tissues
JA Montoya-Zegarra, E Russo, P Runge, M Jadhav, AH Willrodt, S Stoma, SF Nørrelykke, M Detmar, C Halin |
Angiogenesis | 2018 |
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Podoplanin+ tumor lymphatics are rate limiting for breast cancer metastasis
Y Chen, D Keskin, H Sugimoto, K Kanasaki, PE Phillips, L Bizarro, A Sharpe, VS LeBleu, R Kalluri, N Hynes |
PLoS Biology | 2018 |
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Feasibility of diffusion-weighted imaging with DWIBS in staging Hodgkin lymphoma in pediatric patients: comparison with PET/CT
D Baranska, K Matera, M Podgorski, M Gorska-Chrzastek, K Krajewska, J Trelinska, P Grzelak |
Magma (New York, N.Y.) | 2018 |
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[Research Advances of Ang-2 in Non-small Cell Lung Cancer]
Xin Hua, Xiaoli Zhu |
Zhongguo fei ai za zhi = Chinese journal of lung cancer | 2018 |
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Rapamycin reversal of VEGF-C driven lymphatic anomalies in the respiratory tract
Peter Baluk, Li-Chin Yao, Julio C. Flores, Dongwon Choi, Young-Kwon Hong, Donald M. McDonald |
JCI Insight | 2017 |
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Lymphatic Changes in Respiratory Diseases: More than Just Remodeling of the Lung?
B Stump, Y Cui, P Kidambi, AM Lamattina, S El-Chemaly |
American journal of respiratory cell and molecular biology | 2017 |
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Phenotypically heterogeneous podoplanin-expressing cell populations are associated with the lymphatic vessel growth and fibrogenic responses in the acutely and chronically infarcted myocardium
M Cimini, A Cannatá, G Pasquinelli, M Rota, P Goichberg, DK Singla |
PloS one | 2017 |
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Lymphangiogenesis: fuel, smoke, or extinguisher of inflammation’s fire?
GR Abouelkheir, BD Upchurch, JM Rutkowski |
Experimental biology and medicine (Maywood, N.J.) | 2017 |
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Lymphatic Vessels Balance Viral Dissemination and Immune Activation following Cutaneous Viral Infection
CP Loo, NA Nelson, RS Lane, JL Booth, SC Hardin, A Thomas, MK Slifka, JC Nolz, AW Lund |
Cell Reports | 2017 |
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Bone Morphogenetic Proteins in Vascular Homeostasis and Disease
MJ Goumans, A Zwijsen, P ten Dijke, S Bailly |
Cold Spring Harbor perspectives in biology | 2017 |
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FGF-dependent metabolic control of vascular development
P Yu, K Wilhelm, A Dubrac, JK Tung, TC Alves, JS Fang, Y Xie, J Zhu, Z Chen, FD Smet, J Zhang, SW Jin, L Sun, H Sun, RG Kibbey, KK Hirschi, N Hay, P Carmeliet, TW Chittenden, A Eichmann, M Potente, M Simons |
Nature | 2017 |
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Whole-body imaging of lymphovascular niches identifies pre-metastatic roles of midkine
D Olmeda, D Cerezo-Wallis, E Riveiro-Falkenbach, PC Pennacchi, M Contreras-Alcalde, N Ibarz, M Cifdaloz, X Catena, TG Calvo, E Cañón, D Alonso-Curbelo, J Suarez, L Osterloh, O Graña, F Mulero, D Megías, M Cañamero, JL Martínez-Torrecuadrada, C Mondal, JD Martino, D Lora, I Martinez-Corral, JJ Bravo-Cordero, J Muñoz, S Puig, P Ortiz-Romero, JL Rodriguez-Peralto, S Ortega, MS Soengas |
Nature | 2017 |
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Lymph node metastasis and the physicochemical micro-environment of pancreatic ductal adenocarcinoma xeno-grafts
LM Andersen, CS Wegner, TG Simonsen, R Huang, JV Gaustad, A Hauge, K Galappathi, EK Rofstad |
Oncotarget | 2017 |
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"Dicing and Splicing" Sphingosine Kinase and Relevance to Cancer.
Haddadi N, Lin Y, Simpson AM, Nassif NT, McGowan EM |
International journal of molecular sciences | 2017 |
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Foxc1 and Foxc2 deletion causes abnormal lymphangiogenesis and correlates with ERK hyperactivation
Anees Fatima, Ying Wang, Yutaka Uchida, Pieter Norden, Ting Liu, Austin Culver, William Dietz, Ford Culver, Meredith Millay, YOH-SUKE MUKOUYAMA, Tsutomu Kume |
Journal of Clinical Investigation | 2016 |
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Lymphangiogenesis in rat asthma model
A Moldobaeva, J Jenkins, Q Zhong, EM Wagner |
Angiogenesis | 2016 |
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A single dividing cell population with imbalanced fate drives oesophageal tumour growth
J Frede, P Greulich, T Nagy, BD Simons, PH Jones |
Nature Cell Biology | 2016 |
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Differential Receptor Binding and Regulatory Mechanisms for the Lymphangiogenic Growth Factors Vascular Endothelial Growth Factor (VEGF)-C and -D
N Davydova, NC Harris, S Roufail, S Paquet-Fifield, M Ishaq, VA Streltsov, SP Williams, T Karnezis, SA Stacker, MG Achen |
The Journal of biological chemistry | 2016 |
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A Critical Role for Monocytes/Macrophages During Intestinal Inflammation-associated Lymphangiogenesis:
F Becker, E Kurmaeva, FN Gavins, EV Stevenson, AR Navratil, L Jin, I Tsunoda, AW Orr, JS Alexander, DV Ostanin |
Inflammatory Bowel Diseases | 2016 |
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Understanding lymphangiogenesis in knockout models, the cornea, and ocular diseases for the development of therapeutic interventions
JF Yang, A Walia, Y Huang, K Han, MI Rosenblatt, DT Azar, JH Chang |
Survey of Ophthalmology | 2016 |
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The Hepatic Lymphatic Vascular System: Structure, Function, Markers, and Lymphangiogenesis
M Tanaka, Y Iwakiri |
CMGH Cellular and Molecular Gastroenterology and Hepatology | 2016 |
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Phenotypic transformation of intimal and adventitial lymphatics in atherosclerosis: a regulatory role for soluble VEGF receptor 2
M Taher, S Nakao, S Zandi, MI Melhorn, KC Hayes, A Hafezi-Moghadam |
The FASEB Journal | 2016 |
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The Lymphatic System in Disease Processes and Cancer Progression
TP Padera, EF Meijer, LL Munn |
Annual Review of Biomedical Engineering | 2016 |
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Deciphering Pro-Lymphangiogenic Programs during Mammary Involution and Postpartum Breast Cancer
VF Borges, AM Elder, TR Lyons |
Frontiers in Oncology | 2016 |
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Synergistic Effect and Molecular Mechanisms of Traditional Chinese Medicine on Regulating Tumor Microenvironment and Cancer Cells
J Xu, Z Song, Q Guo, J Li |
BioMed Research International | 2016 |
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Human lymphatic endothelial cells contribute to epithelial ovarian carcinoma metastasis by promoting lymphangiogenesis and tumour cell invasion
Y Xie, Y Zhong, T Gao, X Zhang, L Li, H Ruan, D Li |
Experimental and therapeutic medicine | 2016 |
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Combined targeting of TGF-β, EGFR and HER2 suppresses lymphangiogenesis and metastasis in a pancreatic cancer model
J Gore, IE Imasuen-Williams, AM Conteh, KE Craven, M Cheng, M Korc |
Cancer Letters | 2016 |
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Novel application assigned to toluquinol: inhibition of lymphangiogenesis by interfering with VEGF-C/VEGFR-3 signalling pathway: Toluquinol is a novel antilymphangiogenic drug
M García-Caballero, S Blacher, J Paupert, AR Quesada, MA Medina, A Noël |
British Journal of Pharmacology | 2016 |
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OCT-based label-free in vivo lymphangiography within human skin and areola
U Baran, W Qin, X Qi, G Kalkan, RK Wang |
Scientific Reports | 2016 |
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Prevention of Postsurgical Lymphedema by 9-cis Retinoic Acid:
A Bramos, D Perrault, S Yang, E Jung, YK Hong, AK Wong |
Annals of Surgery | 2016 |
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VEGF-D promotes pulmonary oedema in hyperoxic acute lung injury: VEGF-D promotes oedema in hyperoxic lung injury
T Sato, S Paquet-Fifield, NC Harris, S Roufail, DJ Turner, Y Yuan, YF Zhang, SB Fox, ML Hibbs, JL Wilkinson-Berka, RA Williams, SA Stacker, PD Sly, MG Achen |
The Journal of Pathology | 2016 |
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Circulating Angiogenic Factors as Biomarkers of Disease Severity and Bacterial Burden in Pulmonary Tuberculosis
NP Kumar, VV Banurekha, D Nair, S Babu, D Ribatti |
PloS one | 2016 |
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Impaired lymphatic function accelerates cancer growth
ES Steinskog, SJ Sagstad, M Wagner, TV Karlsen, N Yang, CE Markhus, S Yndestad, H Wiig, HP Eikesdal |
Oncotarget | 2016 |
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The nuclear corepressor 1 and the thyroid hormone receptor β suppress breast tumor lymphangiogenesis
O Martínez-Iglesias, D Olmeda, E Alonso-Merino, S Gómez-Rey, AM González-López, E Luengo, MS Soengas, J Palacios, J Regadera, A Aranda |
Oncotarget | 2016 |
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The era of anti-vascular endothelial growth factor (VEGF) drugs in ophthalmology, VEGF and anti-VEGF therapy
D Pożarowska, P Pożarowski |
CENT EUR J IMMUNOL | 2016 |
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DeepCAGE transcriptomics identify HOXD10 as a transcription factor regulating lymphatic endothelial responses to VEGF-C
S Klein, LC Dieterich, A Mathelier, C Chong, A Sliwa-Primorac, YK Hong, JW Shin, M Lizio, M Itoh, H Kawaji, T Lassmann, CO Daub, E Arner, P Carninci, Y Hayashizaki, AR Forrest, WW Wasserman, M Detmar |
Journal of cell science | 2016 |
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HA-ving lymphatics improves lung transplantation
Jonathan Maltzman, Hasina Outtz Reed, Mark L. Kahn |
Journal of Clinical Investigation | 2015 |
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Therapeutic lymphangiogenesis ameliorates established acute lung allograft rejection
Ye Cui, Kaifeng Liu, Maria Elena Monzon, Robert Padera, Hao Wang, Gautam George, Demet Toprak, Elie AbdelNour, Emmanuel D'Agostino, Hilary Goldberg, Mark Perrella, Rosanna Forteza, Ivan Rosas, Gary Visner, Souheil El-Chemaly |
Journal of Clinical Investigation | 2015 |
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The non-canonical role of vascular endothelial growth factor-C axis in cancer progression
CA Wang, SJ Tsai |
Experimental biology and medicine (Maywood, N.J.) | 2015 |
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Lymphatic Vessels, Inflammation, and Immunity in Skin Cancer
AW Lund, TR Medler, SA Leachman, LM Coussens |
Cancer Discovery | 2015 |
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Adrenomedullin in lymphangiogenesis: from development to disease
KR Klein, KM Caron |
Cellular and Molecular Life Sciences | 2015 |
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The lymph node microenvironment and its role in the progression of metastatic cancer
ER Pereira, D Jones, K Jung, TP Padera |
Seminars in Cell & Developmental Biology | 2015 |
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mafba is a downstream transcriptional effector of Vegfc signaling essential for embryonic lymphangiogenesis in zebrafish
K Koltowska, S Paterson, NI Bower, GJ Baillie, AK Lagendijk, JW Astin, H Chen, M Francois, PS Crosier, RJ Taft, C Simons, KA Smith, BM Hogan |
Genes & development | 2015 |
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Culture medium of bone marrow-derived human mesenchymal stem cells effects lymphatic endothelial cells and tumor lymph vessel formation
J Zhan, Y Li, J Yu, Y Zhao, W Cao, J Ma, X Sun, L Sun, H Qian, W Zhu, W Xu |
Oncology Letters | 2015 |
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Rapamycin Protects from Type-I Peritoneal Membrane Failure Inhibiting the Angiogenesis, Lymphangiogenesis, and Endo-MT
GT González-Mateo, AR Aguirre, J Loureiro, H Abensur, P Sandoval, JA Sánchez-Tomero, G Peso, JA Jiménez-Heffernan, V Ruiz-Carpio, R Selgas, M López-Cabrera, A Aguilera, G Liappas |
BioMed Research International | 2015 |
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RASSF8 downregulation promotes lymphangiogenesis and metastasis in esophageal squamous cell carcinoma
Zhang L, Wang JH, Liang RX, Huang ST, Xu J, Yuan LJ, Huang L, Zhou Y, Yu XJ, Wu SY, Luo RZ, Yun JP, Jia WH, Zheng M |
Oncotarget | 2015 |
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Non-caveolar caveolin-1 expression in prostate cancer cells promotes lymphangiogenesis
Nassar ZD, Hill MM, Parton RG, Francois M, Parat MO |
Oncoscience | 2015 |
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Inflammatory lymphangiogenesis in postpartum breast tissue remodeling
Melody A. Swartz |
Journal of Clinical Investigation | 2014 |
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The Schlemm’s canal is a VEGF-C/VEGFR-3 responsive lymphatic-like vessel
Aleksanteri Aspelund, Tuomas Tammela, Salli Antila, Harri Nurmi, Veli-Matti Leppänen, Georgia Zarkada, Lukas Stanczuk, Mathias Francois, Taija Makinen, Pipsa Saharinen, Ilkka Immonen, Kari Alitalo |
Journal of Clinical Investigation | 2014 |
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The lymphatic vasculature revisited
Dontscho Kerjaschki |
Journal of Clinical Investigation | 2014 |
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Corneal Lymphatics: Role in Ocular Inflammation as Inducer and Responder of Adaptive Immunity
SK Chauhan |
Journal of Clinical & Cellular Immunology | 2014 |
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Role of lymphatic vasculature in regional and distant metastases
S Podgrabinska, M Skobe |
Microvascular Research | 2014 |
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Angiopoietin 2 regulates the transformation and integrity of lymphatic endothelial cell junctions
W Zheng, H Nurmi, S Appak, A Sabine, E Bovay, EA Korhonen, F Orsenigo, M Lohela, G D'Amico, T Holopainen, CC Leow, E Dejana, TV Petrova, HG Augustin, K Alitalo |
Genes & development | 2014 |
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Primary and secondary lymphatic valve development: Molecular, functional and mechanical insights
E Bazigou, JT Wilson, JE Moore |
Microvascular Research | 2014 |
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Role of the autonomic nervous system in tumorigenesis and metastasis
C Magnon |
Molecular & Cellular Oncology | 2014 |
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Comprehensive Physiology
R Terjung |
Comprehensive Physiology | 2010 |
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Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd |
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology | 2009 |
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