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JCI - Volume 127, Issue 11
On the cover: Endothelial transplantation revitalizes hematopoietic stem cells. In this month’s JCI, Poulos et al. reveal that the age of bone marrow endothelial cells (BMECs) strongly influences hematopoietic stem cell characteristics. Whereas aged endothelium imparted an aging phenotype to young hematopoietic stem cells, young endothelium rescued many of the deficits observed in aged cells. In the cover image, upregulation of ROS (magenta) represents one age-related defect observed in older BMECs (visualized in red and green with blue nuclei). Image credit: Michael Gutkin. |
Stem Cell Reports - Volume 5, Issue 5
The cover highlights critical cellular components of the bone marrow endothelial niche, which is composed of arteriole and sinusoidal endothelial cells and their LEPR+ perivascular constituents. The vasculature of Vegfr3::YFP (green) and Lepr-cre; TdTomatofl/fl (white) reporter mice were intravitally labeled with an antibody raised against endothelial-specific VECAD, demonstrating discrete bone marrow arteriole (VECAD+VEGFR3−) and sinusoidal (VECAD+VEGFR3+) endothelial niches. Poulos et al. (pp. 881–894) demonstrate that arteriole-derived bone marrow endothelial cells are sufficient to support hematopoietic stem cell maintenance and self-renewal ex vivo, defining a platform that allows for the interrogation of the instructive cellular cross-talk that guides hematopoietic stem cell fate. Image credit: Michael Gutkin |
JCI - Volume 118, Issue 6
Coimmunofluorescence with CD133 (AC133) antibody (red) and EpCAM (a marker of epithelial cells) antibody (green) shows wide distribution of CD133 expression on differentiated epithelium in normal human colon, demonstrating consistency with the murine model. CD133 is expressed by mature luminal ductal epithelial cells in adult organs, including the full spectrum of undifferentiated and differentiated colonic epithelial cells, suggesting that CD133 is not a specific marker of organ-specific stem and progenitor cells. CD133 is widely expressed by differentiated epithelium and that the downregulation of its expression in cancer cells may indicate a transformation of primary CD133+ cancer into more aggressive CD133– metastatic tumors. |
Publications
Ramalingam P, Poulos MG, Gutkin MC, Katsnelson L, Freire AG, Lazzari E, Butler JM. Endothelial mTOR maintains hematopoiesis during aging. Journal of Experimental Medicine. 2020 Jun 1;217(6):e20191212. doi: 10.1084/jem.20191212.
Ramalingam P, Poulos MG, Lazzari E, Gutkin MC, Lopez D, Kloss CC, Crowley MJ, Katsnelson L, Freire AG, Greenblatt MB, Park CY, Butler JM. Chronic activation of endothelial MAPK disrupts hematopoiesis via NFKB dependent inflammatory stress reversible by SCGF. Nature Communications. 2020 Feb 3;11(1):666. doi: 10.1038/s41467-020-14478-8.
Tikhonova AN, Dolgalev I, Hu H, Sivaraj KK, Hoxha E, Cuesta-Domínguez Á, Pinho S, Akhmetzyanova I, Gao J, Witkowski M, Guillamot M, Gutkin MC, Zhang Y, Marier C, Diefenbach C, Kousteni S, Heguy A, Zhong H, Fooksman DR, Butler JM, Economides A, Frenette PS, Adams RH, Satija R, Tsirigos A, Aifantis I. The bone marrow microenvironment at single-cell resolution. Nature. 2019 May;569(7755):222-228. doi: 10.1038/s41586-019-1104-8.
Guo P, Poulos MG, Palikuqi B, Badwe CR, Lis R, Kunar B, Ding BS, Rabbany SY, Shido K, Butler JM, Rafii S. Endothelial jagged-2 sustains hematopoietic stem and progenitor reconstitution after myelosuppression. The journal of clinical investigation. 2017 Oct 23. pii: 92309. doi: 10.1172/JCI92309.
Poulos MG, Ramalingam P, Gutkin MC, Llanos P, Gilleran K, Rabbany SY, Butler JM. Endothelial transplantation rejuvenates aged hematopoietic stem cell function. The journal of clinical investigation. 2017 Nov 1;127(11):4163-4178. doi: 10.1172/JCI93940.
Lis R, Karrasch CC, Poulos MG, Kunar B, Redmond D, Duran JGB, Badwe CR, Schachterle W, Ginsberg M, Xiang J, Tabrizi AR, Shido K, Rosenwaks Z, Elemento O, Speck NA, Butler JM, Scandura JM, Rafii S. Conversion of adult endothelium to immunocompetent haematopoietic stem cells. Nature. 2017 May 25;545(7655):439-445. doi: 10.1038/nature22326.
Lacko LA, Hurtado R, Hinds S, Poulos MG, Butler JM, Stuhlmann H. Altered feto-placental vascularization, feto-placental malperfusion and fetal growth restriction in mice with Egfl7loss of function. Development. 2017 Jul 1;144(13):2469-2479. doi: 10.1242/dev.147025.
Hadland BK, Varnum-Finney B, Mandal PK, Rossi DJ, Poulos MG, Butler JM, Rafii S, Yoder MC, Yoshimoto M, Bernstein ID. A Common Origin for B-1a and B-2 Lymphocytes in Clonal Pre- Hematopoietic Stem Cells. Stem Cell Reports. 2017 Jun 6;8(6):1563-1572. doi: 10.1016/j.stemcr.2017.04.007.
Poulos MG, Ramalingam P, Gutkin MC, Kleppe M, Ginsberg M, Crowley MJP, Elemento O, Levine RL, Rafii S, Kitajewski J, Greenblatt MB, Shim JH, Butler JM. Endothelial-specific inhibition of NF-κB enhances functional haematopoiesis. Nat Commun. 2016 Dec 21;7:13829. doi: 10.1038/ncomms13829.
Kwak H, Salvucci O, Weigert R, Martinez-Torrecuadrada JL, Henkemeyer M, Poulos MG, Butler JM, Tosato G. Sinusoidal ephrin receptor EPHB4 controls hematopoietic progenitor cell mobilization from bone marrow. J Clin Invest. 2016 Dec 1;126(12):4554-4568. doi: 10.1172/JCI87848.
Gori JL, Butler JM, Kunar B, Poulos MG, Ginsberg M, Nolan DJ, Norgaard ZK, Adair JE, Rafii S, Kiem HP. Endothelial Cells Promote Expansion of Long-Term Engrafting Marrow Hematopoietic Stem and Progenitor Cells in Primates. Stem Cells Transl Med. 2017 Mar;6(3):864-876. doi: 10.5966/sctm.2016-0240.
Zewdu R, Risolino M, Barbulescu A, Ramalingam P, Butler JM, Selleri L. Spleen hypoplasia leads to abnormal stress hematopoiesis in mice with loss of Pbx homeoproteins in splenic mesenchyme. J Anat. 2016 Jul;229(1):153-69. doi: 10.1111/joa.12479.
Itkin T, Gur-Cohen S, Spencer JA, Schajnovitz A, Ramasamy SK, Kusumbe AP, Ledergor G, Jung Y, Milo I, Poulos MG, Kalinkovich A, Ludin A, Kollet O, Shakhar G, Butler JM, Rafii S, Adams RH, Scadden DT, Lin CP, Lapidot T. Distinct bone marrow blood vessels differentially regulate haematopoiesis. Nature. 2016 Apr 21;532(7599):323-8. doi: 10.1038/nature17624.
Poulos MG, Crowley MJP, Gutkin MC, Ramalingam P, Schachterle W, Thomas JL, Elemento O, Butler JM. Vascular Platform to Define Hematopoietic Stem Cell Factors and Enhance Regenerative Hematopoiesis. Stem Cell Reports. 2015 Nov 10;5(5):881-894. doi: 10.1016/j.stemcr.2015.08.018.
Hadland BK, Varnum-Finney B, Poulos MG, Moon RT, Butler JM, Rafii S, Bernstein ID. Endothelium and NOTCH specify and amplify aorta-gonad-mesonephros-derived hematopoietic stem cells. J Clin Invest. 2015 May;125(5):2032-45. doi: 10.1172/JCI80137.
Gori JL, Butler JM, Chan YY, Chandrasekaran D, Poulos MG, Ginsberg M, Nolan DJ, Elemento O, Wood BL, Adair JE, Rafii S, Kiem HP. Vascular niche promotes hematopoietic multipotent progenitor formation from pluripotent stem cells. J Clin Invest. 2015 Mar 2;125(3):1243-54. doi: 10.1172/JCI79328.
Poulos MG, Gars EJ, Gutkin MC, Kloss CC, Ginsberg M, Scandura JM, Rafii S, Butler JM. Activation of the vascular niche supports leukemic progression and resistance to chemotherapy. Exp Hematol. 2014 Nov;42(11):976-986.e3. doi: 10.1016/j.exphem.2014.08.003.
Sandler VM, Lis R, Liu Y, Kedem A, James D, Elemento O, Butler JM, Scandura JM, Rafii S. Reprogramming human endothelial cells to haematopoietic cells requires vascular induction. Nature. 2014 Jul 17;511(7509):312-8. doi: 10.1038/nature13547.
Raynaud CM, Butler JM, Halabi NM, Ahmad FS, Ahmed B, Rafii S, Rafii A. Endothelial cells provide a niche for placental hematopoietic stem/progenitor cell expansion through broad transcriptomic modification. Stem Cell Res. 2013 Nov;11(3):1074-90. doi: 10.1016/j.scr.2013.07.010.
Poulos MG, Guo P, Kofler NM, Pinho S, Gutkin MC, Tikhonova A, Aifantis I, Frenette PS, Kitajewski J, Rafii S, Butler JM. Endothelial Jagged-1 is necessary for homeostatic and regenerative hematopoiesis. Cell Rep. 2013 Sep 12;4(5):1022-34. doi: 10.1016/j.celrep.2013.07.048.
Nolan DJ, Ginsberg M, Israely E, Palikuqi B, Poulos MG, James D, Ding BS, Schachterle W, Liu Y, Rosenwaks Z, Butler JM, Xiang J, Rafii A, Shido K, Rabbany SY, Elemento O, Rafii S. Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev Cell. 2013 Jul 29;26(2):204-19. doi: 10.1016/j.devcel.2013.06.017.
Rafii S, Kloss CC, Butler JM, Ginsberg M, Gars E, Lis R, Zhan Q, Josipovic P, Ding BS, Xiang J, Elemento O, Zaninovic N, Rosenwaks Z, Sadelain M, Rafii JA, James D. Human ESC-derived hemogenic endothelial cells undergo distinct waves of endothelial to hematopoietic transition. Blood. 2013 Jan 31;121(5):770-80. doi: 10.1182/blood-2012-07-444208.
Ginsberg M, James D, Ding BS, Nolan D, Geng F, Butler JM, Schachterle W, Pulijaal VR, Mathew S, Chasen ST, Xiang J, Rosenwaks Z, Shido K, Elemento O, Rabbany SY, Rafii S. Efficient direct reprogramming of mature amniotic cells into endothelial cells by ETS factors and TGFβ suppression. Cell. 2012 Oct 26;151(3):559-75. doi: 10.1016/j.cell.2012.09.032.
Butler JM, Gars EJ, James DJ, Nolan DJ, Scandura JM, Rafii S. Development of a vascular niche platform for expansion of repopulating human cord blood stem and progenitor cells. Blood. 2012 Aug 9;120(6):1344-7. doi: 10.1182/blood-2011-12-398115.
Kimura Y, Ding B, Imai N, Nolan DJ, Butler JM, Rafii S. c-Kit-mediated functional positioning of stem cells to their niches is essential for maintenance and regeneration of adult hematopoiesis. PLoS One. 2011;6(10):e26918. doi: 10.1371/journal.pone.0026918.
Ding BS, Nolan DJ, Butler JM, James D, Babazadeh AO, Rosenwaks Z, Mittal V, Kobayashi H, Shido K, Lyden D, Sato TN, Rabbany SY, Rafii S. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature. 2010 Nov 11;468(7321):310-5. doi: 10.1038/nature09493.
Kobayashi H, Butler JM, O'Donnell R, Kobayashi M, Ding BS, Bonner B, Chiu VK, Nolan DJ, Shido K, Benjamin L, Rafii S. Angiocrine factors from Akt-activated endothelial cells balance self-renewal and differentiation of haematopoietic stem cells. Nat Cell Biol. 2010 Nov;12(11):1046-56. doi: 10.1038/ncb2108.
Butler JM, Nolan DJ, Vertes EL, Varnum-Finney B, Kobayashi H, Hooper AT, Seandel M, Shido K, White IA, Kobayashi M, Witte L, May C, Shawber C, Kimura Y, Kitajewski J, Rosenwaks Z, Bernstein ID, Rafii S. Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell. 2010 Mar 5;6(3):251-64. doi: 10.1016/j.stem.2010.02.001.
Madlambayan GJ, Butler JM, Hosaka K, Jorgensen M, Fu D, Guthrie SM, Shenoy AK, Brank A, Russell KJ, Otero J, Siemann DW, Scott EW, Cogle CR. Bone marrow stem and progenitor cell contribution to neovasculogenesis is dependent on model system with SDF-1 as a permissive trigger. Blood. 2009 Nov 5;114(19):4310-9. doi: 10.1182/blood-2009-03-211342.
Hooper AT, Butler JM, Nolan DJ, Kranz A, Iida K, Kobayashi M, Kopp HG, Shido K, Petit I, Yanger K, James D, Witte L, Zhu Z, Wu Y, Pytowski B, Rosenwaks Z, Mittal V, Sato TN, Rafii S. Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell. 2009 Mar 6;4(3):263-74. doi: 10.1016/j.stem.2009.01.006.
Seandel M, Butler JM, Kobayashi H, Hooper AT, White IA, Zhang F, Vertes EL, Kobayashi M, Zhang Y, Shmelkov SV, Hackett NR, Rabbany S, Boyer JL, Rafii S. Generation of a functional and durable vascular niche by the adenoviral E4ORF1 gene. Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19288-93. doi: 10.1073/pnas.0805980105.
Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, St Clair R, Baljevic M, White I, Jin DK, Chadburn A, Murphy AJ, Valenzuela DM, Gale NW, Thurston G, Yancopoulos GD, D'Angelica M, Kemeny N, Lyden D, Rafii S. CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest. 2008 Jun;118(6):2111-20. doi: 10.1172/JCI34401.
Reviews
Freire AG, Butler JM. Blood making: learning what to put into the dish. F1000Res. 2020 Jan 23;9:F1000 Faculty Rev-38. doi: 10.12688/f1000research.21245.1.
Lazzari E, Butler JM. The Instructive Role of the Bone Marrow Niche in Aging and Leukemia. Curr Stem Cell Rep. 2018;4(4):291-298. doi: 10.1007/s40778-018-0143-7.
Ramalingam P, Poulos MG, Butler JM. Regulation of the hematopoietic stem cell lifecycle by the endothelial niche. Curr Opin Hematol. 2017 Jul;24(4):289-299. doi: 10.1097/MOH.0000000000000350.
Rafii S, Ginsberg M, Scandura J, Butler JM, Ding BS. Transplantation of Endothelial Cells to Mitigate Acute and Chronic Radiation Injury to Vital Organs. Radiat Res. 2016 Aug;186(2):196-202. doi: 10.1667/RR14461.1.
Butler JM, Rafii S. Stem cells: Painkillers caught in blood-cell trafficking. Nature. 2013 Mar 21;495(7441):317-8. doi: 10.1038/nature12085.
Butler JM, Rafii S. Generation of a vascular niche for studying stem cell homeostasis. Methods Mol Biol. 2012;904:221-33. doi: 10.1007/978-1-61779-943-3_18.
Butler JM, Kobayashi H, Rafii S. Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat Rev Cancer. 2010 Feb;10(2):138-46. doi: 10.1038/nrc2791.
Ramalingam P, Poulos MG, Gutkin MC, Katsnelson L, Freire AG, Lazzari E, Butler JM. Endothelial mTOR maintains hematopoiesis during aging. Journal of Experimental Medicine. 2020 Jun 1;217(6):e20191212. doi: 10.1084/jem.20191212.
Ramalingam P, Poulos MG, Lazzari E, Gutkin MC, Lopez D, Kloss CC, Crowley MJ, Katsnelson L, Freire AG, Greenblatt MB, Park CY, Butler JM. Chronic activation of endothelial MAPK disrupts hematopoiesis via NFKB dependent inflammatory stress reversible by SCGF. Nature Communications. 2020 Feb 3;11(1):666. doi: 10.1038/s41467-020-14478-8.
Tikhonova AN, Dolgalev I, Hu H, Sivaraj KK, Hoxha E, Cuesta-Domínguez Á, Pinho S, Akhmetzyanova I, Gao J, Witkowski M, Guillamot M, Gutkin MC, Zhang Y, Marier C, Diefenbach C, Kousteni S, Heguy A, Zhong H, Fooksman DR, Butler JM, Economides A, Frenette PS, Adams RH, Satija R, Tsirigos A, Aifantis I. The bone marrow microenvironment at single-cell resolution. Nature. 2019 May;569(7755):222-228. doi: 10.1038/s41586-019-1104-8.
Guo P, Poulos MG, Palikuqi B, Badwe CR, Lis R, Kunar B, Ding BS, Rabbany SY, Shido K, Butler JM, Rafii S. Endothelial jagged-2 sustains hematopoietic stem and progenitor reconstitution after myelosuppression. The journal of clinical investigation. 2017 Oct 23. pii: 92309. doi: 10.1172/JCI92309.
Poulos MG, Ramalingam P, Gutkin MC, Llanos P, Gilleran K, Rabbany SY, Butler JM. Endothelial transplantation rejuvenates aged hematopoietic stem cell function. The journal of clinical investigation. 2017 Nov 1;127(11):4163-4178. doi: 10.1172/JCI93940.
Lis R, Karrasch CC, Poulos MG, Kunar B, Redmond D, Duran JGB, Badwe CR, Schachterle W, Ginsberg M, Xiang J, Tabrizi AR, Shido K, Rosenwaks Z, Elemento O, Speck NA, Butler JM, Scandura JM, Rafii S. Conversion of adult endothelium to immunocompetent haematopoietic stem cells. Nature. 2017 May 25;545(7655):439-445. doi: 10.1038/nature22326.
Lacko LA, Hurtado R, Hinds S, Poulos MG, Butler JM, Stuhlmann H. Altered feto-placental vascularization, feto-placental malperfusion and fetal growth restriction in mice with Egfl7loss of function. Development. 2017 Jul 1;144(13):2469-2479. doi: 10.1242/dev.147025.
Hadland BK, Varnum-Finney B, Mandal PK, Rossi DJ, Poulos MG, Butler JM, Rafii S, Yoder MC, Yoshimoto M, Bernstein ID. A Common Origin for B-1a and B-2 Lymphocytes in Clonal Pre- Hematopoietic Stem Cells. Stem Cell Reports. 2017 Jun 6;8(6):1563-1572. doi: 10.1016/j.stemcr.2017.04.007.
Poulos MG, Ramalingam P, Gutkin MC, Kleppe M, Ginsberg M, Crowley MJP, Elemento O, Levine RL, Rafii S, Kitajewski J, Greenblatt MB, Shim JH, Butler JM. Endothelial-specific inhibition of NF-κB enhances functional haematopoiesis. Nat Commun. 2016 Dec 21;7:13829. doi: 10.1038/ncomms13829.
Kwak H, Salvucci O, Weigert R, Martinez-Torrecuadrada JL, Henkemeyer M, Poulos MG, Butler JM, Tosato G. Sinusoidal ephrin receptor EPHB4 controls hematopoietic progenitor cell mobilization from bone marrow. J Clin Invest. 2016 Dec 1;126(12):4554-4568. doi: 10.1172/JCI87848.
Gori JL, Butler JM, Kunar B, Poulos MG, Ginsberg M, Nolan DJ, Norgaard ZK, Adair JE, Rafii S, Kiem HP. Endothelial Cells Promote Expansion of Long-Term Engrafting Marrow Hematopoietic Stem and Progenitor Cells in Primates. Stem Cells Transl Med. 2017 Mar;6(3):864-876. doi: 10.5966/sctm.2016-0240.
Zewdu R, Risolino M, Barbulescu A, Ramalingam P, Butler JM, Selleri L. Spleen hypoplasia leads to abnormal stress hematopoiesis in mice with loss of Pbx homeoproteins in splenic mesenchyme. J Anat. 2016 Jul;229(1):153-69. doi: 10.1111/joa.12479.
Itkin T, Gur-Cohen S, Spencer JA, Schajnovitz A, Ramasamy SK, Kusumbe AP, Ledergor G, Jung Y, Milo I, Poulos MG, Kalinkovich A, Ludin A, Kollet O, Shakhar G, Butler JM, Rafii S, Adams RH, Scadden DT, Lin CP, Lapidot T. Distinct bone marrow blood vessels differentially regulate haematopoiesis. Nature. 2016 Apr 21;532(7599):323-8. doi: 10.1038/nature17624.
Poulos MG, Crowley MJP, Gutkin MC, Ramalingam P, Schachterle W, Thomas JL, Elemento O, Butler JM. Vascular Platform to Define Hematopoietic Stem Cell Factors and Enhance Regenerative Hematopoiesis. Stem Cell Reports. 2015 Nov 10;5(5):881-894. doi: 10.1016/j.stemcr.2015.08.018.
Hadland BK, Varnum-Finney B, Poulos MG, Moon RT, Butler JM, Rafii S, Bernstein ID. Endothelium and NOTCH specify and amplify aorta-gonad-mesonephros-derived hematopoietic stem cells. J Clin Invest. 2015 May;125(5):2032-45. doi: 10.1172/JCI80137.
Gori JL, Butler JM, Chan YY, Chandrasekaran D, Poulos MG, Ginsberg M, Nolan DJ, Elemento O, Wood BL, Adair JE, Rafii S, Kiem HP. Vascular niche promotes hematopoietic multipotent progenitor formation from pluripotent stem cells. J Clin Invest. 2015 Mar 2;125(3):1243-54. doi: 10.1172/JCI79328.
Poulos MG, Gars EJ, Gutkin MC, Kloss CC, Ginsberg M, Scandura JM, Rafii S, Butler JM. Activation of the vascular niche supports leukemic progression and resistance to chemotherapy. Exp Hematol. 2014 Nov;42(11):976-986.e3. doi: 10.1016/j.exphem.2014.08.003.
Sandler VM, Lis R, Liu Y, Kedem A, James D, Elemento O, Butler JM, Scandura JM, Rafii S. Reprogramming human endothelial cells to haematopoietic cells requires vascular induction. Nature. 2014 Jul 17;511(7509):312-8. doi: 10.1038/nature13547.
Raynaud CM, Butler JM, Halabi NM, Ahmad FS, Ahmed B, Rafii S, Rafii A. Endothelial cells provide a niche for placental hematopoietic stem/progenitor cell expansion through broad transcriptomic modification. Stem Cell Res. 2013 Nov;11(3):1074-90. doi: 10.1016/j.scr.2013.07.010.
Poulos MG, Guo P, Kofler NM, Pinho S, Gutkin MC, Tikhonova A, Aifantis I, Frenette PS, Kitajewski J, Rafii S, Butler JM. Endothelial Jagged-1 is necessary for homeostatic and regenerative hematopoiesis. Cell Rep. 2013 Sep 12;4(5):1022-34. doi: 10.1016/j.celrep.2013.07.048.
Nolan DJ, Ginsberg M, Israely E, Palikuqi B, Poulos MG, James D, Ding BS, Schachterle W, Liu Y, Rosenwaks Z, Butler JM, Xiang J, Rafii A, Shido K, Rabbany SY, Elemento O, Rafii S. Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev Cell. 2013 Jul 29;26(2):204-19. doi: 10.1016/j.devcel.2013.06.017.
Rafii S, Kloss CC, Butler JM, Ginsberg M, Gars E, Lis R, Zhan Q, Josipovic P, Ding BS, Xiang J, Elemento O, Zaninovic N, Rosenwaks Z, Sadelain M, Rafii JA, James D. Human ESC-derived hemogenic endothelial cells undergo distinct waves of endothelial to hematopoietic transition. Blood. 2013 Jan 31;121(5):770-80. doi: 10.1182/blood-2012-07-444208.
Ginsberg M, James D, Ding BS, Nolan D, Geng F, Butler JM, Schachterle W, Pulijaal VR, Mathew S, Chasen ST, Xiang J, Rosenwaks Z, Shido K, Elemento O, Rabbany SY, Rafii S. Efficient direct reprogramming of mature amniotic cells into endothelial cells by ETS factors and TGFβ suppression. Cell. 2012 Oct 26;151(3):559-75. doi: 10.1016/j.cell.2012.09.032.
Butler JM, Gars EJ, James DJ, Nolan DJ, Scandura JM, Rafii S. Development of a vascular niche platform for expansion of repopulating human cord blood stem and progenitor cells. Blood. 2012 Aug 9;120(6):1344-7. doi: 10.1182/blood-2011-12-398115.
Kimura Y, Ding B, Imai N, Nolan DJ, Butler JM, Rafii S. c-Kit-mediated functional positioning of stem cells to their niches is essential for maintenance and regeneration of adult hematopoiesis. PLoS One. 2011;6(10):e26918. doi: 10.1371/journal.pone.0026918.
Ding BS, Nolan DJ, Butler JM, James D, Babazadeh AO, Rosenwaks Z, Mittal V, Kobayashi H, Shido K, Lyden D, Sato TN, Rabbany SY, Rafii S. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature. 2010 Nov 11;468(7321):310-5. doi: 10.1038/nature09493.
Kobayashi H, Butler JM, O'Donnell R, Kobayashi M, Ding BS, Bonner B, Chiu VK, Nolan DJ, Shido K, Benjamin L, Rafii S. Angiocrine factors from Akt-activated endothelial cells balance self-renewal and differentiation of haematopoietic stem cells. Nat Cell Biol. 2010 Nov;12(11):1046-56. doi: 10.1038/ncb2108.
Butler JM, Nolan DJ, Vertes EL, Varnum-Finney B, Kobayashi H, Hooper AT, Seandel M, Shido K, White IA, Kobayashi M, Witte L, May C, Shawber C, Kimura Y, Kitajewski J, Rosenwaks Z, Bernstein ID, Rafii S. Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell. 2010 Mar 5;6(3):251-64. doi: 10.1016/j.stem.2010.02.001.
Madlambayan GJ, Butler JM, Hosaka K, Jorgensen M, Fu D, Guthrie SM, Shenoy AK, Brank A, Russell KJ, Otero J, Siemann DW, Scott EW, Cogle CR. Bone marrow stem and progenitor cell contribution to neovasculogenesis is dependent on model system with SDF-1 as a permissive trigger. Blood. 2009 Nov 5;114(19):4310-9. doi: 10.1182/blood-2009-03-211342.
Hooper AT, Butler JM, Nolan DJ, Kranz A, Iida K, Kobayashi M, Kopp HG, Shido K, Petit I, Yanger K, James D, Witte L, Zhu Z, Wu Y, Pytowski B, Rosenwaks Z, Mittal V, Sato TN, Rafii S. Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell. 2009 Mar 6;4(3):263-74. doi: 10.1016/j.stem.2009.01.006.
Seandel M, Butler JM, Kobayashi H, Hooper AT, White IA, Zhang F, Vertes EL, Kobayashi M, Zhang Y, Shmelkov SV, Hackett NR, Rabbany S, Boyer JL, Rafii S. Generation of a functional and durable vascular niche by the adenoviral E4ORF1 gene. Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19288-93. doi: 10.1073/pnas.0805980105.
Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, St Clair R, Baljevic M, White I, Jin DK, Chadburn A, Murphy AJ, Valenzuela DM, Gale NW, Thurston G, Yancopoulos GD, D'Angelica M, Kemeny N, Lyden D, Rafii S. CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest. 2008 Jun;118(6):2111-20. doi: 10.1172/JCI34401.
Reviews
Freire AG, Butler JM. Blood making: learning what to put into the dish. F1000Res. 2020 Jan 23;9:F1000 Faculty Rev-38. doi: 10.12688/f1000research.21245.1.
Lazzari E, Butler JM. The Instructive Role of the Bone Marrow Niche in Aging and Leukemia. Curr Stem Cell Rep. 2018;4(4):291-298. doi: 10.1007/s40778-018-0143-7.
Ramalingam P, Poulos MG, Butler JM. Regulation of the hematopoietic stem cell lifecycle by the endothelial niche. Curr Opin Hematol. 2017 Jul;24(4):289-299. doi: 10.1097/MOH.0000000000000350.
Rafii S, Ginsberg M, Scandura J, Butler JM, Ding BS. Transplantation of Endothelial Cells to Mitigate Acute and Chronic Radiation Injury to Vital Organs. Radiat Res. 2016 Aug;186(2):196-202. doi: 10.1667/RR14461.1.
Butler JM, Rafii S. Stem cells: Painkillers caught in blood-cell trafficking. Nature. 2013 Mar 21;495(7441):317-8. doi: 10.1038/nature12085.
Butler JM, Rafii S. Generation of a vascular niche for studying stem cell homeostasis. Methods Mol Biol. 2012;904:221-33. doi: 10.1007/978-1-61779-943-3_18.
Butler JM, Kobayashi H, Rafii S. Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat Rev Cancer. 2010 Feb;10(2):138-46. doi: 10.1038/nrc2791.
