Alkylating chemotherapeutic agents cyclophosphamide and melphalan cause functional injury to human bone marrow-derived mesenchymal stem cells

Annals of Hematology

Volumn 90, Issue 7, 2011, Pages 777-789

  Kemp, Kevin ^a,b   Morse, Ruth ^a   Sanders, Kelly ^a   Hows, Jill ^a   Donaldson, Craig ^a  

^a UNIVERSITY OF THE WEST OF ENGLAND   (United Kingdom)

^b FRENCHAY HOSPITAL   (United Kingdom)

Author keywords

Bone marrow; Chemotherapy; Hematopoietic stem cells; Mesenchymal stem cells; Transplantation

Indexed keywords

CD34 ANTIGEN; CYCLOPHOSPHAMIDE; HERMES ANTIGEN; MELPHALAN;

ARTICLE; CELL EXPANSION; CELL MIGRATION; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; DRUG CYTOTOXICITY; FEMUR SHAFT; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS, CD34; ANTINEOPLASTIC AGENTS, ALKYLATING; BONE MARROW CELLS; CELLS, CULTURED; COLONY-FORMING UNITS ASSAY; CYCLOPHOSPHAMIDE; FETAL BLOOD; HUMANS; MELPHALAN; MESENCHYMAL STEM CELLS;

EID: 79960254998     PISSN: 09395555     EISSN: 14320584     Source Type: Journal    
DOI: 10.1007/s00277-010-1141-8     Document Type: Article

References (60)

1. MF Pittenger AM Mackay SC Beck RK Jaiswal R Douglas JD Mosca MA Moorman DW Simonetti S Craig DR Marshak 1999 Multilineage potential of adult human mesenchymal stem cells Science 284 5411 143 147 10.1126/science.284.5411.143 1:CAS:528:DyaK1MXitlCnu7o%3D (Pubitemid 29282067)
2. S Rafii R Mohle F Shapiro BM Frey MA Moore 1997 Regulation of hematopoiesis by microvascular endothelium Leuk Lymphoma 27 5-6 375 386 9477120 1:CAS:528:DC%2BD3cXisFOhsbY%3D (Pubitemid 28029900)
3. MK Majumdar MA Thiede SE Haynesworth SP Bruder SL Gerson 2000 Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages J Hematother Stem Cell Res 9 6 841 848 11177595 10.1089/152581600750062264 1:CAS:528:DC%2BD3MXhtFKgtbg%3D (Pubitemid 32110282)
4. MK Majumdar MA Thiede JD Mosca M Moorman SL Gerson 1998 Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells J Cell Physiol 176 1 57 66 9618145 10.1002/(SICI)1097- 4652(199807)176:1<57::AID-JCP7>3.0.CO;2-7 1:CAS:528:DyaK1cXjsFGkt7c%3D (Pubitemid 28277195)
5. T Ishida M Inaba H Hisha K Sugiura Y Adachi N Nagata R Ogawa RA Good S Ikehara 1994 Requirement of donor-derived stromal cells in the bone marrow for successful allogeneic bone marrow transplantation. Complete prevention of recurrence of autoimmune diseases in MRL/MP-Ipr/Ipr mice by transplantation of bone marrow plus bones (stromal cells) from the same donor J Immunol 152 6 3119 3127 8144907 1:STN:280:DyaK2c7psVSksQ%3D%3D
6. J Domenech F Roingeard O Herault D Truglio I Desbois P Colombat C Binet 1998 Changes in the functional capacity of marrow stromal cells after autologous bone marrow transplantation Leuk Lymphoma 29 5-6 533 546 9643567 10.3109/10428199809050913 1:STN:280:DyaK1czgsFOhsg%3D%3D (Pubitemid 28288719)
7. M Galotto G Berisso L Delfino M Podesta L Ottaggio S Dallorso C Dufour GB Ferrara A Abbondandolo G Dini A Bacigalupo R Cancedda R Quarto 1999 Stromal damage as consequence of high-dose chemo/radiotherapy in bone marrow transplant recipients Exp Hematol 27 9 1460 1466 10480437 10.1016/S0301-472X(99)00076-4 1:STN:280:DyaK1MvgvVeitg%3D%3D (Pubitemid 29409465)
8. E O'Flaherty R Sparrow J Szer 1995 Bone marrow stromal function from patients after bone marrow transplantation Bone Marrow Transplant 15 2 207 212 7539666
9. C Carlo-Stella A Tabilio E Regazzi D Garau R La Tagliata S Trasarti C Andrizzi M Vignetti G Meloni 1997 Effect of chemotherapy for acute myelogenous leukemia on hematopoietic and fibroblast marrow progenitors Bone Marrow Transplant 20 6 465 471 9313879 10.1038/sj.bmt.1700916 1:STN:280: DyaK2svlvFWjtg%3D%3D (Pubitemid 27434894)
10. F Corazza C Hermans A Ferster P Fondu A Demulder E Sariban 2004 Bone marrow stroma damage induced by chemotherapy for acute lymphoblastic leukemia in children Pediatr Res 55 1 152 158 14561785 10.1203/01.PDR.0000099773.71438.91 (Pubitemid 38018705)
11. A Banfi M Podesta L Fazzuoli MR Sertoli M Venturini G Santini R Cancedda R Quarto 2001 High-dose chemotherapy shows a dose-dependent toxicity to bone marrow osteoprogenitors: a mechanism for post-bone marrow transplantation osteopenia Cancer 92 9 2419 2428 11745299 10.1002/1097-0142(20011101)92: 9<2419::AID-CNCR1591>3.0.CO;2-K 1:CAS:528:DC%2BD3MXotl2itb0%3D (Pubitemid 33029088)
12. GI Cohen JS Greenberger GP Canellos 1982 Effect of chemotherapy and irradiation on interactions between stromal and hemopoietic cells in vitro Scan Electron Microsc Pt 1 359 365 7167752 (Pubitemid 13113532)
13. EI Domaratskaia EI Bueverova OD Paiushina VI Starostin 2005 Alkylating damage by dipin of hematopoietic and stromal cells of the bone marrow Izv Akad Nauk Ser Biol 3 267 272 16004256
14. J Domenech E Gihana A Dayan D Truglio C Linassier I Desbois JP Lamagnere P Colombat C Binet 1994 Haemopoiesis of transplanted patients with autologous marrows assessed by long-term marrow culture Br J Haematol 88 3 488 496 7819062 10.1111/j.1365-2141.1994.tb05064.x 1:STN:280:DyaK2M7hvVyhsQ%3D%3D (Pubitemid 24345095)
15. W Fried W Chamberlin A Kedo J Barone 1976 Effects of radiation on hematopoietic stroma Exp Hematol 4 5 310 314 976391 1:STN:280: DyaE2s%2Fis1Wrsg%3D%3D
16. K Kemp R Morse S Wexler C Cox E Mallam J Hows C Donaldson 2010 Chemotherapy-induced mesenchymal stem cell damage in patients with hematological malignancy Ann Hematol 89 7 701 713 20119670 10.1007/s00277-009-0896-2 1:CAS:528:DC%2BC3cXmtlyhsb4%3D
17. PJ Simmons D Przepiorka ED Thomas B Torok-Storb 1987 Host origin of marrow stromal cells following allogeneic bone marrow transplantation Nature 328 6129 429 432 2886914 10.1038/328429a0 1:STN:280:DyaL2s3oslajtw%3D%3D (Pubitemid 17097774)
18. D Cilloni C Carlo-Stella F Falzetti G Sammarelli E Regazzi S Colla V Rizzoli F Aversa MF Martelli A Tabilio 2000 Limited engraftment capacity of bone marrow-derived mesenchymal cells following T-cell-depleted hematopoietic stem cell transplantation Blood 96 10 3637 3643 11071665 1:CAS:528: DC%2BD3cXotFKrs74%3D
19. ON Koc C Peters P Aubourg S Raghavan S Dyhouse R DeGasperi EH Kolodny YB Yoseph SL Gerson HM Lazarus AI Caplan PA Watkins W Krivit 1999 Bone marrow-derived mesenchymal stem cells remain host-derived despite successful hematopoietic engraftment after allogeneic transplantation in patients with lysosomal and peroxisomal storage diseases Exp Hematol 27 11 1675 1681 10560915 10.1016/S0301-472X(99)00101-0 1:STN:280:DC%2BD3c%2FitlGksw%3D%3D (Pubitemid 29526752)
20. WE Fibbe WA Noort F Schipper R Willemze 2001 Ex vivo expansion and engraftment potential of cord blood-derived CD34+ cells in NOD/SCID mice Ann NY Acad Sci 938 9 17 11458530 10.1111/j.1749-6632.2001.tb03569.x 1:CAS:528:DC%2BD3MXlsV2ktLg%3D (Pubitemid 32620013)
21. G Almeida-Porada AW Flake HA Glimp ED Zanjani 1999 Cotransplantation of stroma results in enhancement of engraftment and early expression of donor hematopoietic stem cells in utero Exp Hematol 27 10 1569 1575 10517499 10.1016/S0301-472X(99)00090-9 1:STN:280:DyaK1MvksFSrtQ%3D%3D (Pubitemid 29458432)
22. M Angelopoulou E Novelli JE Grove HM Rinder C Civin L Cheng DS Krause 2003 Cotransplantation of human mesenchymal stem cells enhances human myelopoiesis and megakaryocytopoiesis in NOD/SCID mice Exp Hematol 31 5 413 420 12763140 10.1016/S0301-472X(03)00042-0 1:CAS:528:DC%2BD3sXjvFamt7g%3D (Pubitemid 36579367)
23. PS in't Anker WA Noort AB Kruisselbrink SA Scherjon W Beekhuizen R Willemze HH Kanhai WE Fibbe 2003 Nonexpanded primary lung and bone marrow-derived mesenchymal cells promote the engraftment of umbilical cord blood-derived CD34(+) cells in NOD/SCID mice Exp Hematol 31 10 881 889 10.1016/S0301-472X(03)00202-9 (Pubitemid 37211372)
24. ON Koc SL Gerson BW Cooper SM Dyhouse SE Haynesworth AI Caplan HM Lazarus 2000 Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy J Clin Oncol 18 2 307 316 10637244 1:STN:280:DC%2BD3c7gsFektw%3D%3D (Pubitemid 30056419)
25. SA Wexler C Donaldson P Denning-Kendall C Rice B Bradley JM Hows 2003 Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not Br J Haematol 121 2 368 374 12694261 10.1046/j.1365-2141.2003.04284.x (Pubitemid 36560606)
26. M Dominici K Le Blanc I Mueller I Slaper-Cortenbach F Marini D Krause R Deans A Keating D Prockop E Horwitz 2006 Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement Cytotherapy 8 4 315 317 16923606 10.1080/ 14653240600855905 1:STN:280:DC%2BD28vpvFSjsA%3D%3D (Pubitemid 44269669)
27. TL Chen JL Passos-Coelho DA Noe MJ Kennedy KC Black OM Colvin LB Grochow 1995 Nonlinear pharmacokinetics of cyclophosphamide in patients with metastatic breast cancer receiving high-dose chemotherapy followed by autologous bone marrow transplantation Cancer Res 55 4 810 816 7850794 1:CAS:528: DyaK2MXjsleltrY%3D
28. J Li HK Law YL Lau GC Chan 2004 Differential damage and recovery of human mesenchymal stem cells after exposure to chemotherapeutic agents Br J Haematol 127 3 326 334 15491295 10.1111/j.1365-2141.2004.05200.x 1:CAS:528: DC%2BD2cXhtVentbzE (Pubitemid 39468948)
29. HM Lazarus RH Herzig J Graham-Pole SN Wolff GL Phillips S Strandjord D Hurd W Forman EM Gordon P Coccia, et al. 1983 Intensive melphalan chemotherapy and cryopreserved autologous bone marrow transplantation for the treatment of refractory cancer J Clin Oncol 1 6 359 367 6366139 1:STN:280: DyaL2c7jslyitA%3D%3D (Pubitemid 14181196)
30. F Pinguet P Martel M Fabbro I Petit P Canal S Culine C Astre F Bressolle 1997 Pharmacokinetics of high-dose intravenous melphalan in patients undergoing peripheral blood hematopoietic progenitor-cell transplantation Anticancer Res 17 1B 605 611 9066587 1:CAS:528:DyaK2sXitFSgtLY%3D (Pubitemid 27105535)
31. DS Alberts SY Chang HS Chen BJ Larcom TL Evans 1980 Comparative pharmacokinetics of chlorambucil and melphalan in man Recent Results Cancer Res 74 124 131 7444135 1:STN:280:DyaL3M%2FnvVWjtw%3D%3D
32. PH Rooney C Telfer MC McFadyen WT Melvin GI Murray 2004 The role of cytochrome P450 in cytotoxic bioactivation: future therapeutic directions Curr Cancer Drug Targets 4 3 257 265 15134533 10.2174/1568009043333014 1:CAS:528:DC%2BD2cXjs1Gnu7w%3D (Pubitemid 38560074)
33. Y Nieto WP Vaughan 2004 Pharmacokinetics of high-dose chemotherapy Bone Marrow Transplant 33 3 259 269 14647243 10.1038/sj.bmt.1704353 1:CAS:528:DC%2BD2cXmt12rug%3D%3D (Pubitemid 38256557)
34. JM Hows BA Bradley JC Marsh T Luft L Coutinho NG Testa TM Dexter 1992 Growth of human umbilical-cord blood in longterm haemopoietic cultures Lancet 340 8811 73 76 1352013 10.1016/0140-6736(92)90396-K 1:STN:280: DyaK38zhtVSguw%3D%3D
35. J Cichy E Pure 2003 The liberation of CD44 J Cell Biol 161 5 839 843 12796473 10.1083/jcb.200302098 1:CAS:528:DC%2BD3sXks1Gmu7g%3D (Pubitemid 36718417)
36. S Ghaffari F Smadja-Joffe R Oostendorp JP Levesque G Dougherty A Eaves C Eaves 1999 CD44 isoforms in normal and leukemic hematopoiesis Exp Hematol 27 6 978 993 10378887 10.1016/S0301-472X(99)00023-5 1:CAS:528:DyaK1MXktFensLs%3D (Pubitemid 29275386)
37. J Liu G Jiang 2006 CD44 and hematologic malignancies Cell Mol Immunol 3 5 359 365 17092433 1:CAS:528:DC%2BD28XhtlensLrP
38. H Ponta D Wainwright P Herrlich 1998 The CD44 protein family Int J Biochem Cell Biol 30 3 299 305 9611772 10.1016/S1357-2725(97)00152-0 1:CAS:528:DyaK1cXjtlWhuro%3D (Pubitemid 28234223)
39. RJ Sneath DC Mangham 1998 The normal structure and function of CD44 and its role in neoplasia Mol Pathol 51 4 191 200 9893744 10.1136/mp.51.4.191 1:CAS:528:DyaK1cXmtVyht7o%3D (Pubitemid 28394267)
40. H Zheng X Wang RJ Legerski PM Glazer L Li 2006 Repair of DNA interstrand cross-links: interactions between homology-dependent and homology-independent pathways DNA Repair (Amst) 5 5 566 574 10.1016/j.dnarep.2006.01.010 1:CAS:528:DC%2BD28XjvV2qtbo%3D
41. AD Huitema KD Smits RA Mathot JH Schellens S Rodenhuis JH Beijnen 2000 The clinical pharmacology of alkylating agents in high-dose chemotherapy Anticancer Drugs 11 7 515 533 11036954 10.1097/00001813-200008000-00002 1:CAS:528:DC%2BD3cXnt1yhu7w%3D
42. JH Davies BA Evans ME Jenney JW Gregory 2002 In vitro effects of chemotherapeutic agents on human osteoblast-like cells Calcif Tissue Int 70 5 408 415 12055656 10.1007/s002230020039 1:CAS:528:DC%2BD38Xlt1Knt7Y%3D (Pubitemid 36935443)
43. Z Zhao X Tang Y You W Li F Liu P Zou 2006 Assessment of bone marrow mesenchymal stem cell biological characteristics and support hemotopoiesis function in patients with chronic myeloid leukemia Leuk Res 30 8 993 1003 16448696 10.1016/j.leukres.2005.12.010 1:CAS:528:DC%2BD28Xls1arurY%3D (Pubitemid 43831189)
44. D Hochhauser 1997 Modulation of chemosensitivity through altered expression of cell cycle regulatory genes in cancer Anticancer Drugs 8 10 903 910 9436633 10.1097/00001813-199711000-00001 1:CAS:528:DyaK1cXislSmug%3D%3D (Pubitemid 28027088)
45. S Khaldoyanidi L Sikora I Orlovskaya V Matrosova V Kozlov P Sriramarao 2001 Correlation between nicotine-induced inhibition of hematopoiesis and decreased CD44 expression on bone marrow stromal cells Blood 98 2 303 312 11435297 10.1182/blood.V98.2.303 1:CAS:528:DC%2BD3MXlt1Krtrg%3D
46. J Moll S Khaldoyanidi JP Sleeman M Achtnich I Preuss H Ponta P Herrlich 1998 Two different functions for CD44 proteins in human myelopoiesis J Clin Invest 102 5 1024 1034 9727071 10.1172/JCI2494 1:CAS:528:DyaK1cXlvVCqtLc%3D (Pubitemid 28419247)
47. JS Reese ON Koc SL Gerson 1999 Human mesenchymal stem cells provide stromal support for efficient CD34+ transduction J Hematother Stem Cell Res 8 5 515 523 10791902 10.1089/152581699319966 1:CAS:528:DyaK1MXotVequ74%3D
48. P Szumilas K Barcew M Baskiewicz-Masiuk B Wiszniewska MZ Ratajczak B Machalinski 2005 Effect of stem cell mobilization with cyclophosphamide plus granulocyte colony-stimulating factor on morphology of haematopoietic organs in mice Cell Prolif 38 1 47 61 15679866 10.1111/j.1365-2184.2005.00329.x 1:CAS:528:DC%2BD2MXit1GrtrY%3D (Pubitemid 40229267)
49. Cottler-Fox MH, Lapidot T, Petit I, Kollet O, DiPersio JF, Link D, and Devine S (2003) Stem cell mobilization. Hematology Am Soc Hematol Educ Program, pp 419-437.
50. T Lapidot A Dar O Kollet 2005 How do stem cells find their way home? Blood 106 6 1901 1910 15890683 10.1182/blood-2005-04-1417 1:CAS:528: DC%2BD2MXhtVWksLzJ (Pubitemid 41291700)
51. T Ponomaryov A Peled I Petit RS Taichman L Habler J Sandbank F Arenzana-Seisdedos A Magerus A Caruz N Fujii A Nagler M Lahav M Szyper-Kravitz D Zipori T Lapidot 2000 Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function J Clin Invest 106 11 1331 1339 11104786 10.1172/JCI10329 1:CAS:528:DC%2BD3cXosFKlsL0%3D
52. Y Zhao Y Zhan KA Burke WF Anderson 2005 Soluble factor(s) from bone marrow cells can rescue lethally irradiated mice by protecting endogenous hematopoietic stem cells Exp Hematol 33 4 428 434 15781333 10.1016/j.exphem. 2005.01.003 1:CAS:528:DC%2BD2MXisVCqurY%3D (Pubitemid 40387625)
53. T Lapidot I Petit 2002 Current understanding of stem cell mobilization: the roles of chemokines, proteolytic enzymes, adhesion molecules, cytokines, and stromal cells Exp Hematol 30 9 973 981 12225788 10.1016/S0301-472X(02)00883-4 1:CAS:528:DC%2BD38XmvVCqsrY%3D (Pubitemid 35286613)
54. SJ Collis S Neutzel TL Thompson MJ Swartz LE Dillehay MI Collector SJ Sharkis TL DeWeese 2004 Hematopoietic progenitor stem cell homing in mice lethally irradiated with ionizing radiation at differing dose rates Radiat Res 162 1 48 55 15222777 10.1667/RR3197 1:CAS:528:DC%2BD2cXlslWhtLo%3D (Pubitemid 39044718)
55. PJ Hendrikx CM Martens A Hagenbeek JF Keij JW Visser 1996 Homing of fluorescently labeled murine hematopoietic stem cells Exp Hematol 24 2 129 140 8641334 1:STN:280:DyaK287psFGhtQ%3D%3D (Pubitemid 26096306)
56. A Bacigalupo 2004 Mesenchymal stem cells and haematopoietic stem cell transplantation Best Pract Res Clin Haematol 17 3 387 399 15498711 1:CAS:528:DC%2BD2cXovVKlsbs%3D (Pubitemid 39462571)
57. TM Dexter TD Allen LG Lajtha 1977 Conditions controlling the proliferation of haemopoietic stem cells in vitro J Cell Physiol 91 3 335 344 301143 10.1002/jcp.1040910303 1:STN:280:DyaE2s7ovVSnsQ%3D%3D (Pubitemid 8112206)
58. E de Wynter RE Ploemacher 2001 Assays for the assessment of human hematopoietic stem cells J Biol Regul Homeost Agents 15 1 23 27 11388741 (Pubitemid 32492725)
59. RS Riley M Idowu A Chesney S Zhao J McCarty LS Lamb JM Ben-Ezra 2005 Hematologic aspects of myeloablative therapy and bone marrow transplantation J Clin Lab Anal 19 2 47 79 15756708 10.1002/jcla.20055 (Pubitemid 40389482)
60. EH Javazon KJ Beggs AW Flake 2004 Mesenchymal stem cells: paradoxes of passaging Exp Hematol 32 5 414 425 15145209 10.1016/j.exphem.2004.02.004 1:CAS:528:DC%2BD2cXktVCqtrg%3D (Pubitemid 38624325)