International Journal of Stem Cells

Korean Society for Stem Cell Research (한국줄기세포학회)
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Hematopoietic Stem Cells and Their Roles in Tissue Regeneration

  • Lee, Ji Yoon (CHA Advanced Research Institute, CHA University) ;
  • Hong, Seok-Ho (Department of Internal Medicine, School of Medicine, Kangwon National University)
  • Received : 2019.10.12
  • Accepted : 2019.12.01
  • Published : 2020.03.31
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Abstract

Hematopoietic stem cells (HSCs) are regarded as one of essential cell sources for treating regenerative diseases. Among many stem cells, the feasibility of using adult-derived hematopoietic stem cells in therapeutic approaches is very diverse, and is unarguably regarded as an important cell source in stem cell biology. So far, many investigators are exploring HSCs and modified HSCs for use in clinical and basic science. In the present review, we briefly summarized HSCs and their application in pathophysiologic conditions, including non-hematopoietic tissue regeneration as well as blood disorders. HSCs and HSCs-derived progenitors are promising cell sources in regenerative medicine and their contributions can be properly applied to treat pathophysiologic conditions. Among many adult stem cells, HSCs are a powerful tool to treat patients with diseases such as hematologic malignancies and liver disease. Since HSCs can be differentiated into diverse progenitors including endothelial progenitors, they may be useful for constructing strategies for effective therapy.

Keywords

Acknowledgement

This study was supported by grants from the National Research Foundation (NRF) funded by the Korean government (MSIT) (2019R1A2C2005453), Basic Science Research Program through the NRF funded by the Ministry of Education (2017R1D1A1B03031406) and 2017 Research Grant from Kangwon National University (No. 52017-0448).

References

  1. Till JE, Mcculloch EA. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 1961;14:213-222 https://doi.org/10.2307/3570892
  2. Cheng T, Rodrigues N, Shen H, Yang Y, Dombkowski D, Sykes M, Scadden DT. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 2000;287:1804-1808 https://doi.org/10.1126/science.287.5459.1804
  3. Zhao M, Perry JM, Marshall H, Venkatraman A, Qian P, He XC, Ahamed J, Li L. Megakaryocytes maintain homeostatic quiescence and promote post-injury regeneration of hematopoietic stem cells. Nat Med 2014;20:1321-1326 https://doi.org/10.1038/nm.3706
  4. Ye M, Zhang H, Amabile G, Yang H, Staber PB, Zhang P, Levantini E, Alberich-Jorda M, Zhang J, Kawasaki A, Tenen DG. C/EBPa controls acquisition and maintenance of adult haematopoietic stem cell quiescence. Nat Cell Biol 2013;15:385-394 https://doi.org/10.1038/ncb2698
  5. Seita J, Weissman IL. Hematopoietic stem cell: self-renewal versus differentiation. Wiley Interdiscip Rev Syst Biol Med 2010;2:640-653 https://doi.org/10.1002/wsbm.86
  6. Morrison SJ, Weissman IL. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994;1:661-673 https://doi.org/10.1016/1074-7613(94)90037-X
  7. Mebius RE, Miyamoto T, Christensen J, Domen J, Cupedo T, Weissman IL, Akashi K. The fetal liver counterpart of adult common lymphoid progenitors gives rise to all lymphoid lineages, CD45+CD4+CD3- cells, as well as macrophages. J Immunol 2001;166:6593-6601 https://doi.org/10.4049/jimmunol.166.11.6593
  8. Kim JY, Lee JY, Ha KS, Han ET, Park WS, Min CK, Hong SH. Perivascular cells and NADPH oxidase inhibition partially restore hyperglycemia-induced alterations in hematopoietic stem cell and myeloid-derived suppressor cell populations in the bone marrow. Int J Stem Cells 2018;12:63-72
  9. Thomas ED, Lochte HL Jr, Lu WC, Ferrebee JW. Intravenous infusion of bone marrow in patients receiving radiation and chemotherapy. N Engl J Med 1957;257:491-496 https://doi.org/10.1056/NEJM195709122571102
  10. Thomas ED, Lochte HL Jr, Cannon JH, Sahler OD, Ferrebee JW. Supralethal whole body irradiation and isologous marrow transplantation in man. J Clin Invest 1959;38:1709-1716 https://doi.org/10.1172/JCI103949
  11. Morrison SJ, Wandycz AM, Akashi K, Globerson A, Weissman IL. The aging of hematopoietic stem cells. Nat Med 1996;2:1011-1016 https://doi.org/10.1038/nm0996-1011
  12. Florian MC, Dorr K, Niebel A, Daria D, Schrezenmeier H, Rojewski M, Filippi MD, Hasenberg A, Gunzer M, Scharffetter-Kochanek K, Zheng Y, Geiger H. Cdc42 activity regulates hematopoietic stem cell aging and rejuvenation. Cell Stem Cell 2012;10:520-530 https://doi.org/10.1016/j.stem.2012.04.007
  13. Dorshkind K, Montecino-Rodriguez E, Signer RA. The ageing immune system: is it ever too old to become young again? Nat Rev Immunol 2009;9:57-62 https://doi.org/10.1038/nri2471
  14. Linton PJ, Dorshkind K. Age-related changes in lymphocyte development and function. Nat Immunol 2004;5:133-139 https://doi.org/10.1038/ni1033
  15. Sun D, Luo M, Jeong M, Rodriguez B, Xia Z, Hannah R, Wang H, Le T, Faull KF, Chen R, Gu H, Bock C, Meissner A, Gottgens B, Darlington GJ, Li W, Goodell MA. Epigenomic profiling of young and aged HSCs reveals concerted changes during aging that reinforce self-renewal. Cell Stem Cell 2014;14:673-688 https://doi.org/10.1016/j.stem.2014.03.002
  16. Allsopp RC, Morin GB, Horner JW, DePinho R, Harley CB, Weissman IL. Effect of TERT over-expression on the long-term transplantation capacity of hematopoietic stem cells. Nat Med 2003;9:369-371 https://doi.org/10.1038/nm0403-369
  17. Mohrin M, Shin J, Liu Y, Brown K, Luo H, Xi Y, Haynes CM, Chen D. Stem cell aging. A mitochondrial UPR-mediated metabolic checkpoint regulates hematopoietic stem cell aging. Science 2015;347:1374-1377 https://doi.org/10.1126/science.aaa2361
  18. Cancer Genome Atlas Research Network, Ley TJ, Miller C, Ding L, Raphael BJ, Mungall AJ, Robertson A, Hoadley K, Triche TJ Jr, Laird PW, Baty JD, Fulton LL, Fulton R, Heath SE, Kalicki-Veizer J, Kandoth C, Klco JM, Koboldt DC, Kanchi KL, Kulkarni S, Lamprecht TL, Larson DE, Lin L, Lu C, McLellan MD, McMichael JF, Payton J, Schmidt H, Spencer DH, Tomasson MH, Wallis JW, Wartman LD, Watson MA, Welch J, Wendl MC, Ally A, Balasundaram M, Birol I, Butterfield Y, Chiu R, Chu A, Chuah E, Chun HJ, Corbett R, Dhalla N, Guin R, He A, Hirst C, Hirst M, Holt RA, Jones S, Karsan A, Lee D, Li HI, Marra MA, Mayo M, Moore RA, Mungall K, Parker J, Pleasance E, Plettner P, Schein J, Stoll D, Swanson L, Tam A, Thiessen N, Varhol R, Wye N, Zhao Y, Gabriel S, Getz G, Sougnez C, Zou L, Leiserson MD, Vandin F, Wu HT, Applebaum F, Baylin SB, Akbani R, Broom BM, Chen K, Motter TC, Nguyen K, Weinstein JN, Zhang N, Ferguson ML, Adams C, Black A, Bowen J, Gastier-Foster J, Grossman T, Lichtenberg T, Wise L, Davidsen T, Demchok JA, Shaw KR, Sheth M, Sofia HJ, Yang L, Downing JR, Eley G. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med 2013;368:2059-2074
  19. Sharma S, Gurudutta G. Epigenetic regulation of hematopoietic stem cells. Int J Stem Cells 2016;9:36-43 https://doi.org/10.15283/ijsc.2016.9.1.36
  20. Dimopoulos K, Gimsing P, Gronbaek K. The role of epigenetics in the biology of multiple myeloma. Blood Cancer J 2014;4:e207 https://doi.org/10.1038/bcj.2014.29
  21. Kim MJ, Kim MH, Kim SA, Chang JS. Age-related deterioration of hematopoietic stem cells. Int J Stem Cells 2008;1:55-63 https://doi.org/10.15283/ijsc.2008.1.1.55
  22. Pang WW, Price EA, Sahoo D, Beerman I, Maloney WJ, Rossi DJ, Schrier SL, Weissman IL. Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proc Natl Acad Sci U S A 2011;108:20012-20017 https://doi.org/10.1073/pnas.1116110108
  23. Kuranda K, Vargaftig J, de la Rochere P, Dosquet C, Charron D, Bardin F, Tonnelle C, Bonnet D, Goodhardt M. Age-related changes in human hematopoietic stem/progenitor cells. Aging Cell 2011;10:542-546 https://doi.org/10.1111/j.1474-9726.2011.00675.x
  24. Bhatia S, Robison LL, Francisco L, Carter A, Liu Y, Grant M, Baker KS, Fung H, Gurney JG, McGlave PB, Nademanee A, Ramsay NK, Stein A, Weisdorf DJ, Forman SJ. Late mortality in survivors of autologous hematopoietic-cell transplantation: report from the Bone Marrow Transplant Survivor Study. Blood 2005;105:4215-4222 https://doi.org/10.1182/blood-2005-01-0035
  25. Ford CE, Hamerton JL, Barnes DW, Loutit JF. Cytological identification of radiation-chimaeras. Nature 1956;177:452-454 https://doi.org/10.1038/177452a0
  26. Morstyn G, Nicola NA, Metcalf D. Purification of hemopoietic progenitor cells from human marrow using a fucose-binding lectin and cell sorting. Blood 1980;56:798-805 https://doi.org/10.1182/blood.V56.5.798.798
  27. Attal M, Harousseau JL, Stoppa AM, Sotto JJ, Fuzibet JG, Rossi JF, Casassus P, Maisonneuve H, Facon T, Ifrah N, Payen C, Bataille R. A prospective, randomized trial of autologous bone marrow transplantation and chemotherapy in multiple myeloma. Intergroupe Francais du Myelome. N Engl J Med 1996;335:91-97 https://doi.org/10.1056/NEJM199607113350204
  28. Kanate AS, Kharfan-Dabaja MA, Hamadani M. Controversies and recent advances in hematopoietic cell transplantation for follicular non-hodgkin lymphoma. Bone Marrow Res 2012;2012:897215
  29. Boulad F, Wang X, Qu J, Taylor C, Ferro L, Karponi G, Bartido S, Giardina P, Heller G, Prockop SE, Maggio A, Sadelain M, Riviere I. Safe mobilization of CD34+ cells in adults with β-thalassemia and validation of effective globin gene transfer for clinical investigation. Blood 2014;123:1483-1486 https://doi.org/10.1182/blood-2013-06-507178
  30. Lucarelli G, Isgro A, Sodani P, Gaziev J. Hematopoietic stem cell transplantation in thalassemia and sickle cell anemia. Cold Spring Harb Perspect Med 2012;2:a011825
  31. Biffi A, Montini E, Lorioli L, Cesani M, Fumagalli F, Plati T, Baldoli C, Martino S, Calabria A, Canale S, Benedicenti F, Vallanti G, Biasco L, Leo S, Kabbara N, Zanetti G, Rizzo WB, Mehta NA, Cicalese MP, Casiraghi M, Boelens JJ, Del Carro U, Dow DJ, Schmidt M, Assanelli A, Neduva V, Di Serio C, Stupka E, Gardner J, von Kalle C, Bordignon C, Ciceri F, Rovelli A, Roncarolo MG, Aiuti A, Sessa M, Naldini L. Lentiviral hematopoietic stem cell gene therapy benefits metachromatic leukodystrophy. Science 2013;341:1233158 https://doi.org/10.1126/science.1233158
  32. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275:964-967 https://doi.org/10.1126/science.275.5302.964
  33. Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 2001;105:369-377 https://doi.org/10.1016/S0092-8674(01)00328-2
  34. Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, Wang X, Finegold M, Weissman IL, Grompe M. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 2000;6:1229-1234 https://doi.org/10.1038/81326
  35. Wagers AJ, Sherwood RI, Christensen JL, Weissman IL. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 2002;297:2256-2259 https://doi.org/10.1126/science.1074807
  36. Zaret KS, Grompe M. Generation and regeneration of cells of the liver and pancreas. Science 2008;322:1490-1494 https://doi.org/10.1126/science.1161431
  37. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 1999;5:434-438 https://doi.org/10.1038/7434
  38. Eglitis MA, Mezey E. Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc Natl Acad Sci U S A 1997;94:4080-4085 https://doi.org/10.1073/pnas.94.8.4080
  39. Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, Mavilio F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998;279:1528-1530 https://doi.org/10.1126/science.279.5356.1528
  40. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 1999;85:221-228 https://doi.org/10.1161/01.RES.85.3.221
  41. Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP. Bone marrow as a potential source of hepatic oval cells. Science 1999;284:1168-1170 https://doi.org/10.1126/science.284.5417.1168
  42. Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 2000;290:1779-1782 https://doi.org/10.1126/science.290.5497.1779
  43. Alison MR, Poulsom R, Jeffery R, Dhillon AP, Quaglia A, Jacob J, Novelli M, Prentice G, Williamson J, Wright NA. Hepatocytes from non-hepatic adult stem cells. Nature 2000;406:257 https://doi.org/10.1038/35018642
  44. Orlic D, Kajstura J, Chimenti S, Bodine DM, Leri A, Anversa P. Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann N Y Acad Sci 2001;938:221-229; discussion 229-230
  45. Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 2001;107:1395-1402 https://doi.org/10.1172/JCI12150
  46. Korbling M, Katz RL, Khanna A, Ruifrok AC, Rondon G, Albitar M, Champlin RE, Estrov Z. Hepatocytes and epithelial cells of donor origin in recipients of peripheralblood stem cells. N Engl J Med 2002;346:738-746 https://doi.org/10.1056/NEJMoa3461002
  47. Yoon YS, Wecker A, Heyd L, Park JS, Tkebuchava T, Kusano K, Hanley A, Scadova H, Qin G, Cha DH, Johnson KL, Aikawa R, Asahara T, Losordo DW. Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction. J Clin Invest 2005;115:326-338 https://doi.org/10.1172/JCI200522326
  48. Lee JY, Park C, Cho YP, Lee E, Kim H, Kim P, Yun SH, Yoon YS. Podoplanin-expressing cells derived from bone marrow play a crucial role in postnatal lymphatic neovascularization. Circulation 2010;122:1413-1425 https://doi.org/10.1161/CIRCULATIONAHA.110.941468
  49. Duran JM, Makarewich CA, Sharp TE, Starosta T, Zhu F, Hoffman NE, Chiba Y, Madesh M, Berretta RM, Kubo H, Houser SR. Bone-derived stem cells repair the heart after myocardial infarction through transdifferentiation and paracrine signaling mechanisms. Circ Res 2013;113:539-552 https://doi.org/10.1161/CIRCRESAHA.113.301202
  50. Lee SG, Moon SH, Kim HJ, Lee JY, Park SJ, Chung HM, Ha TY, Song GW, Jung DH, Park H, Kwon TW, Cho YP. Bone marrow-derived progenitor cells in de novo liver regeneration in liver transplant. Liver Transpl 2015;21:1186-1194 https://doi.org/10.1002/lt.24099
  51. Michalopoulos GK, DeFrances MC. Liver regeneration. Science 1997;276:60-66 https://doi.org/10.1126/science.276.5309.60
  52. Kakinuma S, Nakauchi H, Watanabe M. Hepatic stem/progenitor cells and stem-cell transplantation for the treatment of liver disease. J Gastroenterol 2009;44:167-172 https://doi.org/10.1007/s00535-008-2297-z
  53. Taniguchi H, Toyoshima T, Fukao K, Nakauchi H. Presence of hematopoietic stem cells in the adult liver. Nat Med 1996;2:198-203 https://doi.org/10.1038/nm0296-198
  54. Starzl TE. The saga of liver replacement, with particular reference to the reciprocal influence of liver and kidney transplantation (1955-1967). J Am Coll Surg 2002;195:587-610 https://doi.org/10.1016/S1072-7515(02)01498-9
  55. Theise ND, Badve S, Saxena R, Henegariu O, Sell S, Crawford JM, Krause DS. Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 2000;31:235-240 https://doi.org/10.1002/hep.510310135
  56. Shimano K, Satake M, Okaya A, Kitanaka J, Kitanaka N, Takemura M, Sakagami M, Terada N, Tsujimura T. Hepatic oval cells have the side population phenotype defined by expression of ATP-binding cassette transporter ABCG2/BCRP1. Am J Pathol 2003;163:3-9 https://doi.org/10.1016/S0002-9440(10)63624-3
  57. Abkowitz JL. Can human hematopoietic stem cells become skin, gut, or liver cells? N Engl J Med 2002;346:770-772 https://doi.org/10.1056/NEJM200203073461012
  58. Wang X, Willenbring H, Akkari Y, Torimaru Y, Foster M, Al-Dhalimy M, Lagasse E, Finegold M, Olson S, Grompe M. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 2003;422:897-901 https://doi.org/10.1038/nature01531
  59. Terai S, Ishikawa T, Omori K, Aoyama K, Marumoto Y, Urata Y, Yokoyama Y, Uchida K, Yamasaki T, Fujii Y, Okita K, Sakaida I. Improved liver function in patients with liver cirrhosis after autologous bone marrow cell infusion therapy. Stem Cells 2006;24:2292-2298 https://doi.org/10.1634/stemcells.2005-0542
  60. Yannaki E, Anagnostopoulos A, Kapetanos D, Xagorari A, Iordanidis F, Batsis I, Kaloyannidis P, Athanasiou E, Dourvas G, Kitis G, Fassas A. Lasting amelioration in the clinical course of decompensated alcoholic cirrhosis with boost infusions of mobilized peripheral blood stem cells. Exp Hematol 2006;34:1583-1587 https://doi.org/10.1016/j.exphem.2006.06.012
  61. Gaia S, Smedile A, Omede P, Olivero A, Sanavio F, Balzola F, Ottobrelli A, Abate ML, Marzano A, Rizzetto M, Tarella C. Feasibility and safety of G-CSF administration to induce bone marrow-derived cells mobilization in patients with end stage liver disease. J Hepatol 2006;45:13-19 https://doi.org/10.1016/j.jhep.2006.02.018
  62. Gordon MY, Levicar N, Pai M, Bachellier P, Dimarakis I, Al-Allaf F, M'Hamdi H, Thalji T, Welsh JP, Marley SB, Davies J, Dazzi F, Marelli-Berg F, Tait P, Playford R, Jiao L, Jensen S, Nicholls JP, Ayav A, Nohandani M, Farzaneh F, Gaken J, Dodge R, Alison M, Apperley JF, Lechler R, Habib NA. Characterization and clinical application of human CD34+ stem/progenitor cell populations mobilized into the blood by granulocyte colony-stimulating factor. Stem Cells 2006;24:1822-1830 https://doi.org/10.1634/stemcells.2005-0629
  63. Mohamadnejad M, Namiri M, Bagheri M, Hashemi SM, Ghanaati H, Zare Mehrjardi N, Kazemi Ashtiani S, Malekzadeh R, Baharvand H. Phase 1 human trial of autologous bone marrow-hematopoietic stem cell transplantation in patients with decompensated cirrhosis. World J Gastroenterol 2007;13:3359-3363 https://doi.org/10.3748/wjg.v13.i24.3359
  64. Lyra AC, Soares MB, da Silva LF, Fortes MF, Silva AG, Mota AC, Oliveira SA, Braga EL, de Carvalho WA, Genser B, dos Santos RR, Lyra LG. Feasibility and safety of autologous bone marrow mononuclear cell transplantation in patients with advanced chronic liver disease. World J Gastroenterol 2007;13:1067-1073 https://doi.org/10.3748/wjg.v13.i7.1067
  65. Yan L, Han Y, Wang J, Liu J, Hong L, Fan D. Peripheral blood monocytes from patients with HBV related decompensated liver cirrhosis can differentiate into functional hepatocytes. Am J Hematol 2007;82:949-954 https://doi.org/10.1002/ajh.21030
  66. Khan AA, Parveen N, Mahaboob VS, Rajendraprasad A, Ravindraprakash HR, Venkateswarlu J, Rao SG, Narusu ML, Khaja MN, Pramila R, Habeeb A, Habibullah CM. Safety and efficacy of autologous bone marrow stem cell transplantation through hepatic artery for the treatment of chronic liver failure: a preliminary study. Transplant Proc 2008;40:1140-1144 https://doi.org/10.1016/j.transproceed.2008.03.111
  67. Levicar N, Pai M, Habib NA, Tait P, Jiao LR, Marley SB, Davis J, Dazzi F, Smadja C, Jensen SL, Nicholls JP, Apperley JF, Gordon MY. Long-term clinical results of autologous infusion of mobilized adult bone marrow derived CD34+ cells in patients with chronic liver disease. Cell Prolif 2008;41 Suppl 1:115-125
  68. Han Y, Yan L, Han G, Zhou X, Hong L, Yin Z, Zhang X, Wang S, Wang J, Sun A, Liu Z, Xie H, Wu K, Ding J, Fan D. Controlled trials in hepatitis B virus-related decompensate liver cirrhosis: peripheral blood monocyte transplant versus granulocyte-colony-stimulating factor mobilization therapy. Cytotherapy 2008;10:390-396 https://doi.org/10.1080/14653240802129901
  69. Pai M, Zacharoulis D, Milicevic MN, Helmy S, Jiao LR, Levicar N, Tait P, Scott M, Marley SB, Jestice K, Glibetic M, Bansi D, Khan SA, Kyriakou D, Rountas C, Thillainayagam A, Nicholls JP, Jensen S, Apperley JF, Gordon MY, Habib NA. Autologous infusion of expanded mobilized adult bone marrow-derived CD34+ cells into patients with alcoholic liver cirrhosis. Am J Gastroenterol 2008;103:1952-1958 https://doi.org/10.1111/j.1572-0241.2008.01993.x
  70. Salama H, Zekri AR, Bahnassy AA, Medhat E, Halim HA, Ahmed OS, Mohamed G, Al Alim SA, Sherif GM. Autologous CD34+ and CD133+ stem cells transplantation in patients with end stage liver disease. World J Gastroenterol 2010;16:5297-5305 https://doi.org/10.3748/wjg.v16.i42.5297
  71. Kim JK, Park YN, Kim JS, Park MS, Paik YH, Seok JY, Chung YE, Kim HO, Kim KS, Ahn SH, Kim DY, Kim MJ, Lee KS, Chon CY, Kim SJ, Terai S, Sakaida I, Han KH. Autologous bone marrow infusion activates the progenitor cell compartment in patients with advanced liver cirrhosis. Cell Transplant 2010;19:1237-1246 https://doi.org/10.3727/096368910X506863
  72. Lyra AC, Soares MB, da Silva LF, Braga EL, Oliveira SA, Fortes MF, Silva AG, Brustolim D, Genser B, Dos Santos RR, Lyra LG. Infusion of autologous bone marrow mononuclear cells through hepatic artery results in a short-term improvement of liver function in patients with chronic liver disease: a pilot randomized controlled study. Eur J Gastroenterol Hepatol 2010;22:33-42 https://doi.org/10.1097/MEG.0b013e32832eb69a
  73. Khan AA, Shaik MV, Parveen N, Rajendraprasad A, Aleem MA, Habeeb MA, Srinivas G, Raj TA, Tiwari SK, Kumaresan K, Venkateswarlu J, Pande G, Habibullah CM. Human fetal liver-derived stem cell transplantation as supportive modality in the management of end-stage decompensated liver cirrhosis. Cell Transplant 2010;19:409-418 https://doi.org/10.3727/096368909X484707a
  74. Nikeghbalian S, Pournasr B, Aghdami N, Rasekhi A, Geramizadeh B, Hosseini Asl SM, Ramzi M, Kakaei F, Namiri M, Malekzadeh R, Vosough Dizaj A, MalekHosseini SA, Baharvand H. Autologous transplantation of bone marrow-derived mononuclear and CD133(+) cells in patients with decompensated cirrhosis. Arch Iran Med 2011;14:12-17
  75. Saito T, Okumoto K, Haga H, Nishise Y, Ishii R, Sato C, Watanabe H, Okada A, Ikeda M, Togashi H, Ishikawa T, Terai S, Sakaida I, Kawata S. Potential therapeutic application of intravenous autologous bone marrow infusion in patients with alcoholic liver cirrhosis. Stem Cells Dev 2011;20:1503-1510 https://doi.org/10.1089/scd.2011.0074
  76. Amer ME, El-Sayed SZ, El-Kheir WA, Gabr H, Gomaa AA, El-Noomani N, Hegazy M. Clinical and laboratory evaluation of patients with end-stage liver cell failure injected with bone marrow-derived hepatocyte-like cells. Eur J Gastroenterol Hepatol 2011;23:936-941 https://doi.org/10.1097/MEG.0b013e3283488b00
  77. Garg V, Garg H, Khan A, Trehanpati N, Kumar A, Sharma BC, Sakhuja P, Sarin SK. Granulocyte colony-stimulating factor mobilizes CD34(+) cells and improves survival of patients with acute-on-chronic liver failure. Gastroenterology 2012;142:505-512.e1 https://doi.org/10.1053/j.gastro.2011.11.027
  78. Spahr L, Chalandon Y, Terraz S, Kindler V, Rubbia-Brandt L, Frossard JL, Breguet R, Lanthier N, Farina A, Passweg J, Becker CD, Hadengue A. Autologous bone marrow mononuclear cell transplantation in patients with decompensated alcoholic liver disease: a randomized controlled trial. PLoS One 2013;8:e53719 https://doi.org/10.1371/journal.pone.0053719
  79. Andreone P, Catani L, Margini C, Brodosi L, Lorenzini S, Sollazzo D, Nicolini B, Giordano R, Montemurro T, Rizzi S, Dan E, Giudice V, Vigano M, Casadei A, Foschi FG, Malvi D, Bernardi M, Conti F, Lemoli RM. Reinfusion of highly purified CD133+ bone marrow-derived stem/progenitor cells in patients with end-stage liver disease: A phase I clinical trial. Dig Liver Dis 2015;47:1059-1066 https://doi.org/10.1016/j.dld.2015.08.018
  80. King A, Barton D, Beard HA, Than N, Moore J, Corbett C, Thomas J, Guo K, Guha I, Hollyman D, Stocken D, Yap C, Fox R, Forbes SJ, Newsome PN. Repeated AutoLogous Infusions of STem cells In Cirrhosis (REALISTIC): a multicentre, phase II, open-label, randomised controlled trial of repeated autologous infusions of granulocyte colonystimulating factor (GCSF) mobilised CD133+ bone marrow stem cells in patients with cirrhosis. A study protocol for a randomised controlled trial. BMJ Open 2015;5:e007700 https://doi.org/10.1136/bmjopen-2015-007700
  81. Sharma M, Rao PN, Sasikala M, Kuncharam MR, Reddy C, Gokak V, Raju B, Singh JR, Nag P, Nageshwar Reddy D. Autologous mobilized peripheral blood CD34(+) cell infusion in non-viral decompensated liver cirrhosis. World J Gastroenterol 2015;21:7264-7271 https://doi.org/10.3748/wjg.v21.i23.7264
  82. Mohamadnejad M, Vosough M, Moossavi S, Nikfam S, Mardpour S, Akhlaghpoor S, Ashrafi M, Azimian V, Jarughi N, Hosseini SE, Moeininia F, Bagheri M, Sharafkhah M, Aghdami N, Malekzadeh R, Baharvand H. Intraportal infusion of bone marrow mononuclear or CD133+ cells in patients with decompensated cirrhosis: a double-blind randomized controlled trial. Stem Cells Transl Med 2016;5:87-94 https://doi.org/10.5966/sctm.2015-0004
  83. Yu SJ, Yoon JH, Kim W, Lee JM, Lee YB, Cho Y, Lee DH, Lee M, Yoo JJ, Cho EJ, Lee JH, Kim YJ, Kim CY. Ultrasound-guided percutaneous portal transplantation of peripheral blood monocytes in patients with liver cirrhosis. Korean J Intern Med 2017;32:261-268 https://doi.org/10.3904/kjim.2015.267

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