Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1
Abstract
The trafficking of circulating stem and progenitor cells to areas of tissue damage is poorly understood. The chemokine stromal cell-derived factor-1 (SDF-1 or CXCL12) mediates homing of stem cells to bone marrow by binding to CXCR4 on circulating cells. SDF-1 and CXCR4 are expressed in complementary patterns during embryonic organogenesis and guide primordial stem cells to sites of rapid vascular expansion. However, the regulation of SDF-1 and its physiological role in peripheral tissue repair remain incompletely understood. Here we show that SDF-1 gene expression is regulated by the transcription factor hypoxia-inducible factor-1 (HIF-1) in endothelial cells, resulting in selective in vivo expression of SDF-1 in ischemic tissue in direct proportion to reduced oxygen tension. HIF-1-induced SDF-1 expression increases the adhesion, migration and homing of circulating CXCR4-positive progenitor cells to ischemic tissue. Blockade of SDF-1 in ischemic tissue or CXCR4 on circulating cells prevents progenitor cell recruitment to sites of injury. Discrete regions of hypoxia in the bone marrow compartment also show increased SDF-1 expression and progenitor cell tropism. These data show that the recruitment of CXCR4-positive progenitor cells to regenerating tissues is mediated by hypoxic gradients via HIF-1-induced expression of SDF-1.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Other hypoxia-induced pro-angiogenic factors include PDGF-β, ANGPT2, and SDF-1α, all of which promote neoangiogenesis.
“Other hypoxia-induced pro-angiogenic factors include platelet-derived growth factor-β (PDGF-β) (Kelly et al., 2003), angiopoietin-2 (ANGPT2) (Kelly et al., 2003), and stromal-derived factor 1α (SDF-1α) (Ceradini et al., 2004), all of which promote neoangiogenesis.”
From Therapeutic targeting of hypoxia and hypoxia-inducible factors in cancer (2016) · cites this paper as Ceradini et al., 2004
Activation of HIF-1α and formation of the HIF complex induce angiogenic growth factor genes including VEGF and SDF-1/CXCL12.
“The activation of HIF-1α and the formation of the HIF complex induce several angiogenic growth factor genes, including VEGF and stromal cell-derived factor-1 (SDF-1)/C-X-C motif chemokine 12 (CXCL12) [82,83,84].”
From The Pathogenesis of Adenomyosis vis-à-vis Endometriosis (2020) · cites this paper as [83]
Cites
Isolation of Putative Progenitor Endothelial Cells for Angiogenesis
Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., Witzenbichler, B., Schatteman, G., & Isner, J. M. (1997) · Science · doi:10.1126/science.275.5302.964 · Cited by 8,725 · see citing works
Targeting HIF-1 for cancer therapy
Semenza, G. L. (2003) · Nature Reviews Cancer · doi:10.1038/nrc1187 · Cited by 6,717 · see citing works
Involvement of chemokine receptors in breast cancer metastasis
Müller, A., Homey, B., Soto, H., Ge, N., Catron, D., Buchanan, M. E., McClanahan, T., Murphy, E., Yuan, W., Wagner, S. N., et al. (2001) · Nature · doi:10.1038/35065016 · Cited by 5,340 · see citing works
Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1
Forsythe, J. A., Jiang, B.-H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D., & Semenza, G. L. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.9.4604 · Cited by 3,981 · see citing works
Circulating endothelial progenitor cells, vascular function, and cardiovascular risk
Hill, J. M., Zalos, G., Halcox, J. P. J., Schenke, W. H., Waclawiw, M. A., Quyyumi, A. A., & Finkel, T. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa022287 · Cited by 3,423 · see citing works
Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development
Zou, Y.-R., Kottmann, A. H., Kuroda, M., Taniuchi, I., & Littman, D. R. (1998) · Nature · doi:10.1038/31269 · Cited by 2,494 · see citing works
Takahashi, T., Kalka, C., Masuda, H., Chen, D., Silver, M., Kearney, M., Magner, M., Isner, J. M., & Asahara, T. (1999) · Nature Medicine · doi:10.1038/7434 · Cited by 2,421 · see citing works
Nagasawa, T., Hirota, S., Tachibana, K., Takakura, N., Nishikawa, S.-I., Kitamura, Y., Yoshida, N., Kikutani, H., & Kishimoto, T. (1996) · Nature · doi:10.1038/382635a0 · Cited by 2,338 · see citing works
Huang, L. E., Gu, J., Schau, M., & Bunn, H. F. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.14.7987 · Cited by 2,113 · see citing works
Dependence of Human Stem Cell Engraftment and Repopulation of NOD/SCID Mice on CXCR4
Peled, A., Petit, I., Kollet, O., Magid, M., Ponomaryov, T., Byk, T., Nagler, A., Ben-Hur, H., Many, A., Shultz, L., et al. (1999) · Science · doi:10.1126/science.283.5403.845 · Cited by 1,644 · see citing works
Tepper, O. M., Galiano, R. D., Capla, J. M., Kalka, C., Gagne, P. J., Jacobowitz, G. R., Levine, J. P., & Gurtner, G. C. (2002) · Circulation · doi:10.1161/01.cir.0000039526.42991.93 · Cited by 1,447 · see citing works
Self-citationAskari, A. T., Unzek, S., Popović, Z., Goldman, C. K., Forudi, F., Kiedrowski, M. J., Rovner, A., Ellis, S. G., Thomas, J. D., DiCorleto, P. E., et al. (2003) · The Lancet · doi:10.1016/s0140-6736(03)14232-8 · Cited by 1,269 · see citing works
Therapeutic Potential of Ex Vivo Expanded Endothelial Progenitor Cells for Myocardial Ischemia
Kawamoto, A., Gwon, H.-C., Iwaguro, H., Yamaguchi, J.-I., Uchida, S., Masuda, H., Silver, M., Ma, H., Kearney, M., Isner, J. M., et al. (2001) · Circulation · doi:10.1161/01.cir.103.5.634 · Cited by 1,219 · see citing works
Dimmeler, S., Aicher, A., Vasa‐Nicotera, M., Mildner-Rihm, C., Adler, K., Tiemann, M., Rütten, H., Fichtlscherer, S., Martin, H., & Zeiher, A. M. (2001) · Journal of Clinical Investigation · doi:10.1172/jci13152 · Cited by 1,206 · see citing works
Yamaguchi, J.-I., Kusano, K. F., Masuo, O., Kawamoto, A., Silver, M., Murasawa, S., Bosch‐Marcé, M., Masuda, H., Losordo, D. W., Isner, J. M., et al. (2003) · Circulation · doi:10.1161/01.cir.0000055313.77510.22 · Cited by 1,149 · see citing works
Dimmeler, S., Aicher, A., Vasa‐Nicotera, M., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci200113152 · Cited by 1,025 · see citing works
Chemokines and the Arrest of Lymphocytes Rolling Under Flow Conditions
Campbell, J. J., Hedrick, J. A., Zlotnik, A., Siani, M. A., Thompson, D. A., & Butcher, E. C. (1998) · Science · doi:10.1126/science.279.5349.381 · Cited by 994 · see citing works
Chemokine receptor CXCR4 downregulated by von Hippel–Lindau tumour suppressor pVHL
Staller, P., Sulitkova, J., Lisztwan, J., Moch, H., Oakeley, E. J., & Krek, W. (2003) · Nature · doi:10.1038/nature01874 · Cited by 870 · see citing works
HGF, SDF-1, and MMP-9 are involved in stress-induced human CD34+ stem cell recruitment to the liver
Kollet, Ó., Shivtiel, S., Chen, Y.-Q., Suriawinata, J., Thung, S. N., Dabeva, M. D., Kahn, J., Spiegel, A., Dar, A., Samira, S., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17902 · Cited by 593 · see citing works
Peled, A., Grabovsky, V., Habler, L., Sandbank, J., Arenzana-Seisdedos, F., Petit, I., Ben‐Hur, H., Lapidot, T., & Alon, R. (1999) · Journal of Clinical Investigation · doi:10.1172/jci7615 · Cited by 550 · see citing works
Hattori, K., Heissig, B., Tashiro, K., Honjo, T., Tateno, M., Shieh, J.-H., Hackett, N. R., Quitoriano, M., Crystal, R. G., Rafii, S., et al. (2001) · Blood · doi:10.1182/blood.v97.11.3354 · Cited by 529 · see citing works
Embryonic Expression and Function of the Chemokine SDF-1 and Its Receptor, CXCR4
McGrath, K. E., Koniski, A. D., Maltby, K. M., McGann, J. K., & Palis, J. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9405 · Cited by 466 · see citing works
Signoret, N. Y. M., Oldridge, J., Pelchen–Matthews, A., Klasse, P. J., Tran, T. T., Brass, L. F., ROSENKILDE, M. M., Schwartz, T. W., Holmes, W. D., Dallas, W. S., et al. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.3.651 · Cited by 375 · see citing works
Oxygen saturation in the bone marrow of healthy volunteers
Harrison, J. S., Rameshwar, P., Chang, V. T.-S., & Bandari, P. S. (2002) · Blood · doi:10.1182/blood.v99.1.394 · Cited by 328 · see citing works
Amara, A., Lorthioir, O., Valenzuela-Fernández, A., Magérus, A., Thelen, M., Montes, M., Virelizier, J., Delepierre, M., Baleux, F., Lortat‐Jacob, H., et al. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.34.23916 · Cited by 323 · see citing works
Rivard, A., Berthou-Soulié, L., Principe, N., Kearney, M., Curry, C., Branellec, D., Semenza, G. L., & Isner, J. M. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001029200 · Cited by 305 · see citing works
Elson, D. A., Thurston, G., Huang, E. L., Ginzinger, D. G., McDonald, D. M., Johnson, R. S., & Arbeit, J. M. (2001) · Genes & Development · doi:10.1101/gad.914801 · Cited by 297 · see citing works
Ratajczak, M. Z., Majka, M., Kucia, M., Drukała, J., Pietrzkowski, Z. J., Peiper, S. C., & Janowska‐Wieczorek, A. (2003) · Stem Cells · doi:10.1634/stemcells.21-3-363 · Cited by 280 · see citing works
Hitchon, C. A., Wong, K., Ma, G., Reed, J., Lyttle, D., & El-Gabalawy, H. S. (2002) · Arthritis & Rheumatism · doi:10.1002/art.10520 · Cited by 247 · see citing works
Sweeney, E. A., Lortat‐Jacob, H., Priestley, G. V., Nakamoto, B., & Papayannopoulou, T. (2002) · Blood · doi:10.1182/blood.v99.1.44 · Cited by 223 · see citing works
Reiss, K., Mentlein, R., Sievers, J., & Hartmann, D. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00307-x · Cited by 169 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Orimo, A., Gupta, P. B., Sgroi, D. C., Arenzana-Seisdedos, F., Delaunay, T., Naeem, R., Carey, V. J., Richardson, A. L., & Weinberg, R. A. (2005) · Cell · doi:10.1016/j.cell.2005.02.034 · Cited by 3,759 · see citing works
Modes of resistance to anti-angiogenic therapy
Bergers, G., & Hanahan, D. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2442 · Cited by 2,953 · see citing works
“Evidence that low oxygen tension triggers the recruitment of BMDCs stems from observations in experimentally induced ischaemic tissue, wherein endothelial progenitors and other CXCR4 + BMDCs are recruited, in part through increases in HIF1α and its downstream effectors SDF1α (a CXCR4 ligand) and VEGF itsel”
BackgroundThe biology of fracture healing
Marsell, R., & Einhorn, T. A. (2011) · Injury · doi:10.1016/j.injury.2011.03.031 · Cited by 1,824 · see citing works
Hypoxia and the extracellular matrix: drivers of tumour metastasis
Gilkes, D. M., Semenza, G. L., & Wirtz, D. (2014) · Nature Reviews Cancer · doi:10.1038/nrc3726 · Cited by 1,520 · see citing works
Trophic macrophages in development and disease
Pollard, J. W. (2009) · Nature Reviews Immunology · doi:10.1038/nri2528 · Cited by 1,178 · see citing works
Direct measurement of local oxygen concentration in the bone marrow of live animals
Spencer, J. A., Ferraro, F., Roussakis, E., Klein, A., Wu, J., Runnels, J. M., Zaher, W., Mortensen, L. J., Alt, C., Turcotte, R., et al. (2014) · Nature · doi:10.1038/nature13034 · Cited by 1,167 · see citing works
The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages.
Allavena, P., Sica, A., Solinas, G., Porta, C., & Mantovani, A. (2008) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2007.07.004 · Cited by 1,044 · see citing works
Integration of Oxygen Signaling at the Consensus HRE
Wenger, R. H., Stiehl, D. P., & Camenisch, G. (2005) · Science's STKE · doi:10.1126/stke.3062005re12 · Cited by 1,032 · see citing works
Regulation of Oxygen Homeostasis by Hypoxia-Inducible Factor 1
Semenza, G. L. (2009) · Physiology · doi:10.1152/physiol.00045.2008 · Cited by 926 · see citing works
Jang, Y.-Y., & Sharkis, S. J. (2007) · Blood · doi:10.1182/blood-2007-05-087759 · Cited by 894 · see citing works
Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia
Parmar, K., Mauch, P., Vergilio, J.-A., Sackstein, R., & Down, J. D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701152104 · Cited by 867 · see citing works
The role of hypoxia-inducible factors in tumorigenesis
Rankin, E. B., & Giaccia, A. J. (2008) · Cell Death & Differentiation · doi:10.1038/cdd.2008.21 · Cited by 806 · see citing works
Therapeutic targeting of hypoxia and hypoxia-inducible factors in cancer
Wigerup, C., Påhlman, S., & Bexell, D. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.04.009 · Cited by 687 · see citing works
“, 2003), and stromal-derived factor 1α (SDF-1α) (Ceradini et al., 2004), all of which promote neoangiogenesis.”
BackgroundAdult haematopoietic stem cell niches
Crane, G. M., Jeffery, E., & Morrison, S. J. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.53 · Cited by 712 · see citing works
Macrophage polarization in pathology
Sica, A., Erreni, M., Allavena, P., & Porta, C. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1995-y · Cited by 673 · see citing works
Tumor microenvironment: The role of the tumor stroma in cancer
Li, H., Fan, X., & Houghton, J. (2007) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21159 · Cited by 646 · see citing works
Prabhakar, N. R., & Semenza, G. L. (2012) · Physiological Reviews · doi:10.1152/physrev.00030.2011 · Cited by 641 · see citing works
Zimna, A., & Kurpisz, M. (2015) · BioMed Research International · doi:10.1155/2015/549412 · Cited by 604 · see citing works
Cancer related inflammation: the macrophage connection
Sica, A., Allavena, P., & Mantovani, A. (2008) · Cancer Letters · doi:10.1016/j.canlet.2008.03.028 · Cited by 601 · see citing works
Cellular biology of fracture healing
Bahney, C. S., Zondervan, R. L., Allison, P., Theologis, A., Ashley, J. W., Ahn, J., Miclau, T., Marcucio, R. S., & Hankenson, K. D. (2019) · Journal of Orthopaedic Research · doi:10.1002/jor.24170 · Cited by 577 · see citing works
Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1
Semenza, G. L. (2007) · Biochemical Journal · doi:10.1042/bj20070389 · Cited by 541 · see citing works
Macrophage Polarization in Chronic Inflammatory Diseases: Killers or Builders?
Parisi, L., Gini, E., Baci, D., Tremolati, M., Fanuli, M., Bassani, B., Farronato, G., Bruno, A., & Mortara, L. (2018) · Journal of Immunology Research · doi:10.1155/2018/8917804 · Cited by 508 · see citing works
Stabilization of HIF-1α is critical to improve wound healing in diabetic mice
Botusan, I. R., Sunkari, V. G., Savu, O., Catrina, A. I., Grünler, J., Lindberg, S., Pereira, T., Ylä-Herttuala, S., Poellinger, L., Brismar, K., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805230105 · Cited by 533 · see citing works
Vascular endothelium – Gatekeeper of vessel health
Cahill, P. A., & Redmond, E. M. (2016) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2016.03.007 · Cited by 518 · see citing works
The Role of Hypoxia-Inducible Factor in Wound Healing
Hong, W. X., Hu, M. S., Esquivel, M., Liang, G. Y., Rennert, R. C., McArdle, A., Paik, K. J., Duscher, D., Gurtner, G. C., Lorenz, H. P., et al. (2014) · Advances in Wound Care · doi:10.1089/wound.2013.0520 · Cited by 448 · see citing works
Self-citationAging and disease as modifiers of efficacy of cell therapy
Dimmeler, S., & Leri, A. (2008) · Circulation Research · doi:10.1161/circresaha.108.175943 · Cited by 379 · see citing works
Oxidative stress promotes myofibroblast differentiation and tumour spreading
Toullec, A., Gerald, D., Despouy, G., Bourachot, B., Cardon, M., Lefort, S., Richardson, M., Rigaill, G., Parrini, M., Lucchesi, C., et al. (2010) · EMBO Molecular Medicine · doi:10.1002/emmm.201000073 · Cited by 339 · see citing works
Hong, H. S., Lee, J., Lee, E., Kwon, Y. S., Lee, E., Ahn, W., Jiang, M. H., Kim, J. C., & Son, Y. (2009) · Nature Medicine · doi:10.1038/nm.1909 · Cited by 349 · see citing works
Keeley, T. P., & Mann, G. E. (2019) · Physiological Reviews · doi:10.1152/physrev.00041.2017 · Cited by 329 · see citing works
Angiogenic Role of LYVE-1–Positive Macrophages in Adipose Tissue
Cho, C.-H., Jun Koh, Y., Han, J., Sung, H.-K., Jong Lee, H., Morisada, T., Schwendener, R. A., Brekken, R. A., Kang, G., Oike, Y., et al. (2007) · Circulation Research · doi:10.1161/01.res.0000259564.92792.93 · Cited by 309 · see citing works
Lee, K., Qian, D. Z., Rey, S., Wei, H., Liu, J. O., & Semenza, G. L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812801106 · Cited by 289 · see citing works
RetractedRole of hypoxia-inducible factors in breast cancer metastasis
Gilkes, D. M., & Semenza, G. L. (2013) · Future Oncology · doi:10.2217/fon.13.92 · Cited by 274 · see citing works
Hur, J., Yang, H.-M., Yoon, C.-H., Lee, C.-S., Park, K.-W., Kim, J.-H., Kim, T.-Y., Kim, J.-Y., Kang, H.-J., Chae, I.-H., et al. (2007) · Circulation · doi:10.1161/circulationaha.107.694778 · Cited by 255 · see citing works
Radical medicine: treating ageing to cure disease
Finkel, T. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1763 · Cited by 234 · see citing works
Chang, E. I., Loh, S. A., Ceradini, D. J., Chang, E. I., Lin, S.-E., Bastidas, N., Aarabi, S., Chan, D. A., Freedman, M. L., Giaccia, A. J., et al. (2007) · Circulation · doi:10.1161/circulationaha.107.715847 · Cited by 206 · see citing works
Self-citationChemokines as mediators of neovascularization
Keeley, E. C., Mehrad, B., & Strieter, R. M. (2008) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.108.162925 · Cited by 192 · see citing works
Hypoxia-regulated microRNAs in human cancer
Shen, G., Li, X., Jia, Y.-F., Piazza, G. A., & Xi, Y. (2013) · Acta Pharmacologica Sinica · doi:10.1038/aps.2012.195 · Cited by 164 · see citing works
The Pathogenesis of Adenomyosis vis-à-vis Endometriosis
Guo, S.-W. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020485 · Cited by 165 · see citing works
Short-term physiological hypoxia potentiates the therapeutic function of mesenchymal stem cells
Antebi, B., Rodriguez, L. A., Walker, K. P., Asher, A. M., Kamucheka, R. M., Alvarado, L., Mohammadipoor, A., & Cancio, L. C. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-1007-x · Cited by 137 · see citing works
Hypoxia Inducible Factor Pathway Inhibitors as Anticancer Therapeutics
Burroughs, S. K., Kaluz, S., Wang, D., Wang, K., Van Meir, E. G., & Wang, B. (2013) · Future Medicinal Chemistry · doi:10.4155/fmc.13.17 · Cited by 140 · see citing works
Vasculogenesis: A new piece of the endometriosis puzzle
Laschke, M. W., Giebels, C., & Menger, M. D. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr023 · Cited by 136 · see citing works
The role of hypoxia-inducible factor-2 in digestive system cancers
Zhao, J., Du, F., Shen, G., Zheng, F., & Xu, B. (2015) · Cell Death & Disease · doi:10.1038/cddis.2014.565 · Cited by 122 · see citing works
Perrotta, S., Nobili, B., Ferraro, M., Migliaccio, C., Borriello, A., Cucciolla, V., Martinelli, V., Rossi, F., Punzo, F., Cirillo, P., et al. (2006) · Blood · doi:10.1182/blood-2005-06-2422 · Cited by 93 · see citing works
Support of Tumor Endothelial Cells by Chemokine Receptors
Salazar, N., & Zabel, B. A. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00147 · Cited by 72 · see citing works
Hypoxia pathway proteins and their impact on the blood vasculature
Rodriguez, D., Watts, D., Gaete, D., Sormendi, S., & Wielockx, B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179191 · Cited by 62 · see citing works
Dong, F., Khalil, M., Kiedrowski, M., O'Connor, C., Petrovic, E., Zhou, X., & Penn, M. S. (2010) · Circulation Research · doi:10.1161/circresaha.109.208967 · Cited by 44 · see citing works
Sub-anesthetic Xenon Increases Erythropoietin Levels in Humans: A Randomized Controlled Trial
Stoppe, C., Ney, J., Brenke, M., Goetzenich, A., Emontzpohl, C., Schälte, G., Grottke, O., Moeller, M., Rossaint, R., & Coburn, M. (2016) · Sports Medicine · doi:10.1007/s40279-016-0505-1 · Cited by 31 · see citing works
Substance P enhances EPC mobilization for accelerated wound healing
Um, J., Jung, N., Chin, S., Cho, Y., Choi, S., & Park, K. (2016) · Wound Repair and Regeneration · doi:10.1111/wrr.12403 · Cited by 32 · see citing works
Prevention of liver fibrosis and liver reconstitution of DMN‐treated rat liver by transplanted EPCs
Nakamura, T., Torimura, T., Iwamoto, H., Masuda, H., Naitou, M., Koga, H., Abe, M., Hashimoto, O., Tsutsumi, V., Ueno, T., et al. (2012) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2011.02637.x · Cited by 27 · see citing works
HIF gene expression in cancer therapy
Chan, D. A., Krieg, A. J., Turcotte, S., & Giaccia, A. J. (2007) · Methods in Enzymology · doi:10.1016/s0076-6879(07)35016-7 · Cited by 26 · see citing works
Sun, W., Chen, Y., Wang, Y., Luo, P., Zhang, M., Zhang, H., & Hu, P. (2018) · The Analyst · doi:10.1039/c8an01216d · Cited by 25 · see citing works
Kim, K. Y., Lee, H. K., Kim, H., Kim, Y., Kim, Y., Choi, H. H., Kim, S. W., Kim, H. K., & Chae, H. S. (2020) · Medicine · doi:10.1097/md.0000000000020539 · Cited by 7 · see citing works
- Authors
- Ceradini, D. J., Kulkarni, A. R., Callaghan, M. J., Tepper, O. M., Bastidas, N., Kleinman, M. E., Capla, J. M., Galiano, R. D., Levine, J. P., & Gurtner, G. C.
- Affiliations
- NYU Langone Health (US)
- Corresponding author
- Gurtner, Geoffrey C
- ORCID
- Venue
- Nature Medicine
- Published
- 2004-07-04
- Volume
- 10
- Issue
- 8
- Pages
- 858-864
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- OpenAlex
- W1982861439
- Cited by
- 2,600
- References
- 31
- Citations by year
- 2026: 35 · 2025: 52 · 2024: 59 · 2023: 68 · 2022: 65 · 2021: 78 · 2020: 83 · 2019: 106 · 2018: 122 · 2017: 124 · 2016: 131 · 2015: 154 · 2014: 163 · 2013: 169 · 2012: 182
- FWCI
- 55.95
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Sarnoff Cardiovascular Research Foundation
- National Institutes of Health
- National Institute of Biomedical Imaging and Bioengineering (EB002265, R21EB002265)
- Topics
- Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Keywords
- HIF-1, CXCL12, CXCR4, ischemic tissue repair, stem cell homing, endothelial cells, bone marrow, tissue regeneration
- MeSH terms
- Analysis of Variance, Animals, Bone Marrow, Cell Adhesion, Cell Movement, Disease Models, Animal, DNA-Binding Proteins, Enzyme-Linked Immunosorbent Assay, Gene Expression Regulation, Ischemia, Mice, Nude, Nuclear Proteins, Precipitin Tests, Stem Cells, Transcription Factors, Cell Hypoxia, In Situ Hybridization, Receptors, CXCR4, Chemokines, CXC, Reverse Transcriptase Polymerase Chain Reaction, Endothelial Cells, Mice, Hypoxia-Inducible Factor 1, Hypoxia-Inducible Factor 1, alpha Subunit, Chemokine CXCL12
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review