ARTEMIS stabilizes the genome and modulates proliferative responses in multipotent mesenchymal cells

BMC Biology

Volumn 8, Issue , 2010, Pages

  Maas, Sarah A ^a,b   Donghia, Nina M ^a   Tompkins, Kathleen ^a,c   Foreman, Oded ^d   Mills, Kevin D ^a,e  

^a JACKSON LABORATORY   (United States)

^b Adnexus Therapeutics   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d JACKSON LABORATORY   (United States)

^e Maine Medical Research Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUS;

DCLRE1C PROTEIN, HUMAN; NUCLEAR PROTEIN;

ANIMAL; ARTICLE; CELL PROLIFERATION; CYTOLOGY; DNA REPAIR; GENE EXPRESSION PROFILING; GENETICS; GENOMIC INSTABILITY; HUMAN; MESENCHYMAL STEM CELL; METABOLISM; MOUSE; MULTIPOTENT STEM CELL; PHYSIOLOGY; SARCOMA; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

ANIMALS; CELL PROLIFERATION; DNA REPAIR; GENE EXPRESSION PROFILING; GENES, TUMOR SUPPRESSOR; GENOMIC INSTABILITY; HUMANS; MESENCHYMAL STEM CELLS; MICE; MULTIPOTENT STEM CELLS; NUCLEAR PROTEINS; SARCOMA; SIGNAL TRANSDUCTION;

EID: 77958460939     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-8-132     Document Type: Article

References (73)

1. Mills KD, Ferguson DO, Alt FW. The role of DNA breaks in genomic instability and tumorigenesis. Immunol Rev 2003, 194:77-95. 10.1034/j.1600-065X.2003.00060.x, 12846809.
2. Valerie K, Povirk LF. Regulation and mechanisms of mammalian double-strand break repair. Oncogene 2003, 22:5792-5812. 10.1038/sj.onc.1206679, 12947387.
3. Rooney S, Chaudhuri J, Alt FW. The role of the non-homologous end-joining pathway in lymphocyte development. Immunol Rev 2004, 200:115-131. 10.1111/j.0105-2896.2004.00165.x, 15242400.
4. Zhu C, Mills KD, Ferguson DO, Lee C, Manis J, Fleming J, Gao Y, Morton CC, Alt FW. Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell 2002, 109:811-821. 10.1016/S0092-8674(02)00770-5, 12110179.
5. Moshous D, Pannetier C, Chasseval Rd R, Deist Fl F, Cavazzana-Calvo M, Romana S, Macintyre E, Canioni D, Brousse N, Fischer A, Casanova JL, Villartay JP. Partial T and B lymphocyte immunodeficiency and predisposition to lymphoma in patients with hypomorphic mutations in Artemis. J Clin Invest 2003, 111:381-387. 151863, 12569164.
6. Sharpless NE, Ferguson DO, O'Hagan RC, Castrillon DH, Lee C, Farazi PA, Alson S, Fleming J, Morton CC, Frank K, Chin L, Alt FW, DePinho RA. Impaired nonhomologous end-joining provokes soft tissue sarcomas harboring chromosomal translocations, amplifications, and deletions. Mol Cell 2001, 8:1187-1196. 10.1016/S1097-2765(01)00425-7, 11779495.
7. Yan CT, Kaushal D, Murphy M, Zhang Y, Datta A, Chen C, Monroe B, Mostoslavsky G, Coakley K, Gao Y, Mills KD, Fazeli AP, Tepsuporn S, Hall G, Mulligan R, Fox E, Bronson R, De Girolami U, Lee C, Alt FW. XRCC4 suppresses medulloblastomas with recurrent translocations in p53-deficient mice. Proc Natl Acad Sci USA 2006, 103:7378-7383. 10.1073/pnas.0601938103, 1464348, 16670198.
8. Woo Y, Wright SM, Maas SA, Alley TL, Caddle LB, Kamdar S, Affourtit J, Foreman O, Akeson EC, Shaffer D, Bronson RT, Morse HC, Roopenian D, Mills KD. The nonhomologous end joining factor Artemis suppresses multi-tissue tumor formation and prevents loss of heterozygosity. Oncogene 2007, 26:6010-6020. 10.1038/sj.onc.1210430, 17384673.
9. Jeggo P, O'Neill P. The Greek Goddess, Artemis, reveals the secrets of her cleavage. DNA Repair (Amsterdam) 2002, 1:771-777.
10. Moshous D, Callebaut I, de Chasseval R, Corneo B, Cavazzana-Calvo M, Le Deist F, Tezcan I, Sanal O, Bertrand Y, Philippe N, Fischer A, de Villartay JP. Artemis, a Novel DNA double-strand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 2001, 105:177-186. 10.1016/S0092-8674(01)00309-9, 11336668.
11. Zhang X, Zhu Y, Geng L, Wang H, Legerski RJ. Artemis is a negative regulator of p53 in response to oxidative stress. Oncogene 2009, 28:2196-2204. 10.1038/onc.2009.100, 2692457, 19398950.
12. Wang H, Zhang X, Geng L, Teng L, Legerski RJ. Artemis regulates cell cycle recovery from the S phase checkpoint by promoting degradation of cyclin E. J Biol Chem 2009, 284:18236-18243. 10.1074/jbc.M109.002584, 2709338, 19423708.
13. Geng L, Zhang X, Zheng S, Legerski RJ. Artemis links ATM to G2/M checkpoint recovery via regulation of Cdk1-cyclin B. Mol Cell Biol 2007, 27:2625-2635. 10.1128/MCB.02072-06, 1899901, 17242184.
14. Zhang X, Succi J, Feng Z, Prithivirajsingh S, Story MD, Legerski RJ. Artemis is a phosphorylation target of ATM and ATR and is involved in the G2/M DNA damage checkpoint response. Mol Cell Biol 2004, 24:9207-9220. 10.1128/MCB.24.20.9207-9220.2004, 517881, 15456891.
15. Richie CT, Peterson C, Lu T, Hittelman WN, Carpenter PB, Legerski RJ. hSnm1 colocalizes and physically associates with 53BP1 before and after DNA damage. Mol Cell Biol 2002, 22:8635-8647. 10.1128/MCB.22.24.8635-8647.2002, 139863, 12446782.
16. Li L, Moshous D, Zhou Y, Wang J, Xie G, Salido E, Hu D, de Villartay JP, Cowan MJ. A founder mutation in Artemis, an SNM1-like protein, causes SCID in Athabascan-speaking Native Americans. J Immunol 2002, 168:6323-6329.
17. Noordzij JG, Verkaik NS, van der Burg M, van Veelen LR, de Bruin-Versteeg S, Wiegant W, Vossen JM, Weemaes CM, de Groot R, Zdzienicka MZ, van Gent DC, van Dongen JJ. Radiosensitive SCID patients with Artemis gene mutations show a complete B-cell differentiation arrest at the pre-B-cell R checkpoint in bone marrow. Blood 2003, 101:1446-1452. 10.1182/blood-2002-01-0187, 12406895.
18. Villa A, Sobacchi C, Vezzoni P. Omenn syndrome in the context of other B cell-negative severe combined immunodeficiencies. Isr Med Assoc J 2002, 4:218-221.
19. Reger RL, Tucker AH, Wolfe MR. Differentiation and characterization of human MSCs. Methods Mol Biol 2008, 449:93-107. full_text, 18370086.
20. Phinney DG, Prockop DJ. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair: current views. Stem Cells 2007, 25:2896-2902. 10.1634/stemcells.2007-0637, 17901396.
21. Dennis JE, Charbord P. Origin and differentiation of human and murine stroma. Stem Cells 2002, 20:205-214. 10.1634/stemcells.20-3-205, 12004079.
22. Minguell JJ, Erices A, Conget P. Mesenchymal stem cells. Exp Biol Med (Maywood) 2001, 226:507-520.
23. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147. 10.1126/science.284.5411.143, 10102814.
24. Barrilleaux B, Phinney DG, Prockop DJ, O'Connor KC. Review: ex vivo engineering of living tissues with adult stem cells. Tissue Eng 2006, 12:3007-3019. 10.1089/ten.2006.12.3007, 17518617.
25. Gregory CA, Prockop DJ, Spees JL. Non-hematopoietic bone marrow stem cells: molecular control of expansion and differentiation. Exp Cell Res 2005, 306:330-335. 10.1016/j.yexcr.2005.03.018, 15925588.
26. Rooney S, Sekiguchi J, Zhu C, Cheng HL, Manis J, Whitlow S, DeVido J, Foy D, Chaudhuri J, Lombard D, Alt FW. Leaky SCID phenotype associated with defective V(D)J coding end processing in Artemis-deficient mice. Mol Cell 2002, 10:1379-1390. 10.1016/S1097-2765(02)00755-4, 12504013.
27. Jacks T, Remington L, Williams BO, Schmitt EM, Halachmi S, Bronson RT, Weinberg RA. Tumor spectrum analysis in p53-mutant mice. Curr Biol 1994, 4:1-7. 10.1016/S0960-9822(00)00002-6, 7922305.
28. Harvey M, McArthur MJ, Montgomery CA, Butel JS, Bradley A, Donehower LA. Spontaneous and carcinogen-induced tumorigenesis in p53-deficient mice. Nat Genet 1993, 5:225-229. 10.1038/ng1193-225, 8275085.
29. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA, Butel JS, Bradley A. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 1992, 356:215-221. 10.1038/356215a0, 1552940.
30. Rooney S, Sekiguchi J, Whitlow S, Eckersdorff M, Manis JP, Lee C, Ferguson DO, Alt FW. Artemis and p53 cooperate to suppress oncogenic N-myc amplification in progenitor B cells. Proc Natl Acad Sci USA 2004, 101:2410-2415. 10.1073/pnas.0308757101, 356964, 14983023.
31. Meng GZ, Zhang HY, Zhang Z, Wei B, Bu H. Myofibroblastic sarcoma vs nodular fasciitis: a comparative study of chromosomal imbalances. Am J Clin Pathol 2009, 131:701-709. 10.1309/AJCPV6H2WSYXLKFB, 19369631.
32. Isaka T, Nestor AL, Takada T, Allison DC. Chromosomal variations within aneuploid cancer lines. J Histochem Cytochem 2003, 51:1343-1353.
33. Lauwers GY, Grant LD, Donnelly WH, Meloni AM, Foss RM, Sanberg AA, Langham MR. Hepatic undifferentiated (embryonal) sarcoma arising in a mesenchymal hamartoma. Am J Surg Pathol 1997, 21:1248-1254. 10.1097/00000478-199710000-00018, 9331300.
34. Hoogerwerf WA, Hawkins AL, Perlman EJ, Griffin CA. Chromosome analysis of nine osteosarcomas. Genes Chromosomes Cancer 1994, 9:88-92. 10.1002/gcc.2870090203, 7513549.
35. Travis JA, Bridge JA. Significance of both numerical and structural chromosomal abnormalities in clear cell sarcoma. Cancer Genet Cytogenet 1992, 64:104-106. 10.1016/0165-4608(92)90337-8, 1486557.
36. Vanden Berg E, Molenaar WM, Hoekstra HJ, Kamps WA, de Jong B. DNA ploidy and karyotype in recurrent and metastatic soft tissue sarcomas. Mod Pathol 1992, 5:505-514.
37. Sreekantaiah C, Leong SP, Davis JR, Sandberg AA. Cytogenetic and flow cytometric analysis of a clear cell chondrosarcoma. Cancer Genet Cytogenet 1991, 52:193-199. 10.1016/0165-4608(91)90463-5, 2021921.
38. Hiddemann W, Roessner A, Wormann B, Mellin W, Klockenkemper B, Bosing T, Buchner T, Grundmann E. Tumor heterogeneity in osteosarcoma as identified by flow cytometry. Cancer 1987, 59:324-328. 10.1002/1097-0142(19870115)59:2<324::AID-CNCR2820590226>3.0.CO;2-9, 3467822.
39. Potluri VR, Gilbert F. A cytogenetic study of embryonal rhabdomyosarcoma. Cancer Genet Cytogenet 1985, 14:169-173. 10.1016/0165-4608(85)90228-6, 3965122.
40. Smith A, Roberts C, van Haaften-Day C, den Dulk G, Russell P, Tattersall MH. Cytogenetic findings in cell lines derived from four ovarian carcinomas. Cancer Genet Cytogenet 1987, 24:231-242. 10.1016/0165-4608(87)90104-X, 3466675.
41. Gilbert F. Solid tumors of children: chromosome abnormalities and the development of cancer. J Cell Physiol Suppl 1984, 3:165-170. 10.1002/jcp.1041210419, 6086684.
42. Rooney S, Alt FW, Lombard D, Whitlow S, Eckersdorff M, Fleming J, Fugmann S, Ferguson DO, Schatz DG, Sekiguchi J. Defective DNA repair and increased genomic instability in Artemis-deficient murine cells. J Exp Med 2003, 197:553-565. 10.1084/jem.20021891, 2193825, 12615897.
43. Reger RL, Wolfe MR. Freezing harvested hMSCs and recovery of hMSCs from frozen vials for subsequent expansion, analysis, and experimentation. Methods Mol Biol 2008, 449:109-116. full_text, 18370087.
44. Potier E, Ferreira E, Meunier A, Sedel L, Logeart-Avramoglou D, Petite H. Prolonged hypoxia concomitant with serum deprivation induces massive human mesenchymal stem cell death. Tissue Eng 2007, 13:1325-1331. 10.1089/ten.2006.0325, 17518749.
45. Zhu W, Chen J, Cong X, Hu S, Chen X. Hypoxia and serum deprivation-induced apoptosis in mesenchymal stem cells. Stem Cells 2006, 24:416-425. 10.1634/stemcells.2005-0121, 16253984.
46. Cleton-Jansen AM, Anninga JK, Briaire-de Bruijn IH, Romeo S, Oosting J, Egeler RM, Gelderblom H, Taminiau AH, Hogendoorn PC. Profiling of high-grade central osteosarcoma and its putative progenitor cells identifies tumourigenic pathways. Br J Cancer 2009, 101:1909-1918. 10.1038/sj.bjc.6605405, 19888226.
47. Courtwright A, Siamakpour-Reihani S, Arbiser JL, Banet N, Hilliard E, Fried L, Livasy C, Ketelsen D, Nepal DB, Perou CM, Patterson C, Klauber-Demore N. Secreted frizzle-related protein 2 stimulates angiogenesis via a calcineurin/NFAT signaling pathway. Cancer Res 2009, 69:4621-4628. 10.1158/0008-5472.CAN-08-3402, 2699405, 19458075.
48. Enomoto M, Hayakawa S, Itsukushima S, Ren DY, Matsuo M, Tamada K, Oneyama C, Okada M, Takumi T, Nishita M, Minami Y. Autonomous regulation of osteosarcoma cell invasiveness by Wnt5a/Ror2 signaling. Oncogene 2009, 28:3197-3208. 10.1038/onc.2009.175, 19561643.
49. Hou CH, Hsiao YC, Fong YC, Tang CH. Bone morphogenetic protein-2 enhances the motility of chondrosarcoma cells via activation of matrix metalloproteinase-13. Bone 2009, 44:233-242. 10.1016/j.bone.2008.09.021, 19038372.
50. Kansara M, Tsang M, Kodjabachian L, Sims NA, Trivett MK, Ehrich M, Dobrovic A, Slavin J, Choong PF, Simmons PJ, Dawid IB, Thomas DM. Wnt inhibitory factor 1 is epigenetically silenced in human osteosarcoma, and targeted disruption accelerates osteosarcomagenesis in mice. J Clin Invest 2009, 119:837-851. 10.1172/JCI37175, 2662557, 19307728.
51. Karim RZ, Gerega SK, Yang YH, Horvath L, Spillane A, Carmalt H, Scolyer RA, Lee CS. Proteins from the Wnt pathway are involved in the pathogenesis and progression of mammary phyllodes tumours. J Clin Pathol 2009, 62:1016-1020. 10.1136/jcp.2009.066977, 19861560.
52. Kurihara S, Oda Y, Ohishi Y, Kaneki E, Kobayashi H, Wake N, Tsuneyoshi M. Coincident expression of beta-catenin and cyclin D1 in endometrial stromal tumors and related high-grade sarcomas. Mod Pathol 2009, 23:225-34. 10.1038/modpathol.2009.162, 19898427.
53. Chen K, Fallen S, Abaan HO, Hayran M, Gonzalez C, Wodajo F, MacDonald T, Toretsky JA, Uren A. Wnt10b induces chemotaxis of osteosarcoma and correlates with reduced survival. Pediatr Blood Cancer 2008, 51:349-355. 10.1002/pbc.21595, 18465804.
54. Fong YC, Li TM, Wu CM, Hsu SF, Kao ST, Chen RJ, Lin CC, Liu SC, Wu CL, Tang CH. BMP-2 increases migration of human chondrosarcoma cells via PI3K/Akt pathway. J Cell Physiol 2008, 217:846-855. 10.1002/jcp.21568, 18720410.
55. Guo Y, Xie J, Rubin E, Tang YX, Lin F, Zi X, Hoang BH. Frzb, a secreted Wnt antagonist, decreases growth and invasiveness of fibrosarcoma cells associated with inhibition of Met signaling. Cancer Res 2008, 68:3350-3360. 10.1158/0008-5472.CAN-07-3220, 2824245, 18451162.
56. Luo X, Chen J, Song WX, Tang N, Luo J, Deng ZL, Sharff KA, He G, Bi Y, He BC, Bennett E, Huang J, Kang Q, Jiang W, Su Y, Zhu GH, Yin H, He Y, Wang Y, Souris JS, Chen L, Zuo GW, Montag AG, Reid RR, Haydon RC, Luu HH, He TC. Osteogenic BMPs promote tumor growth of human osteosarcomas that harbor differentiation defects. Lab Invest 2008, 88:1264-1277. 10.1038/labinvest.2008.98, 18838962.
57. Matushansky I, Maki RG, Cordon-Cardo C. A context dependent role for Wnt signaling in tumorigenesis and stem cells. Cell Cycle 2008, 7:720-724. 10.4161/cc.7.6.5569, 18239459.
58. Bhat RA, Stauffer B, Komm BS, Bodine PV. Structure-function analysis of secreted frizzled-related protein-1 for its Wnt antagonist function. J Cell Biochem 2007, 102:1519-1528. 10.1002/jcb.21372, 17471511.
59. Dong YF, Soung do Y, Schwarz EM, O'Keefe RJ, Drissi H. Wnt induction of chondrocyte hypertrophy through the Runx2 transcription factor. J Cell Physiol 2006, 208:77-86. 10.1002/jcp.20656, 16575901.
60. Sotobori T, Ueda T, Myoui A, Yoshioka K, Nakasaki M, Yoshikawa H, Itoh K. Bone morphogenetic protein-2 promotes the haptotactic migration of murine osteoblastic and osteosarcoma cells by enhancing incorporation of integrin beta1 into lipid rafts. Exp Cell Res 2006, 312:3927-3938. 10.1016/j.yexcr.2006.08.024, 17022972.
61. Weiss KR, Cooper GM, Jadlowiec JA, McGough RL, Huard J. VEGF and BMP expression in mouse osteosarcoma cells. Clin Orthop Relat Res 2006, 450:111-117. 10.1097/01.blo.0000229333.98781.56, 16906080.
62. Baird K, Davis S, Antonescu CR, Harper UL, Walker RL, Chen Y, Glatfelter AA, Duray PH, Meltzer PS. Gene expression profiling of human sarcomas: insights into sarcoma biology. Cancer Res 2005, 65:9226-9235. 10.1158/0008-5472.CAN-05-1699, 16230383.
63. Chandar N, Swindle J, Szajkovics A, Kolman K. Relationship of bone morphogenetic protein expression during osteoblast differentiation to wild type p53. J Orthop Res 2005, 23:1345-1353.
64. Yoshikawa H, Nakase T, Myoui A, Ueda T. Bone morphogenetic proteins in bone tumors. J Orthop Sci 2004, 9:334-340. 10.1007/s00776-004-0764-9, 15168194.
65. Gobbi G, Sangiorgi L, Lenzi L, Casadei R, Canaider S, Strippoli P, Lucarelli E, Ghedini I, Donati D, Fabbri N, Warzecha J, Yeoung C, Helman LJ, Picci P, Carinci P. Seven BMPs and all their receptors are simultaneously expressed in osteosarcoma cells. Int J Oncol 2002, 20:143-147.
66. Sulzbacher I, Birner P, Trieb K, Pichlbauer E, Lang S. The expression of bone morphogenetic proteins in osteosarcoma and its relevance as a prognostic parameter. J Clin Pathol 2002, 55:381-385. 1769652, 11986346.
67. Miura M, Miura Y, Padilla-Nash HM, Molinolo AA, Fu B, Patel V, Seo BM, Sonoyama W, Zheng JJ, Baker CC, Chen W, Ried T, Shi S. Accumulated chromosomal instability in murine bone marrow mesenchymal stem cells leads to malignant transformation. Stem Cells 2006, 24:1095-1103. 10.1634/stemcells.2005-0403, 16282438.
68. Tolar J, Nauta AJ, Osborn MJ, Panoskaltsis Mortari A, McElmurry RT, Bell S, Xia L, Zhou N, Riddle M, Schroeder TM, Westendorf JJ, McIvor RS, Hogendoorn PC, Szuhai K, Oseth L, Hirsch B, Yant SR, Kay MA, Peister A, Prockop DJ, Fibbe WE, Blazar BR. Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 2007, 25:371-379. 10.1634/stemcells.2005-0620, 17038675.
69. Charytonowicz E, Cordon-Cardo C, Matushansky I, Ziman M. Alveolar rhabdomyosarcoma: is the cell of origin a mesenchymal stem cell?. Cancer Lett 2009, 279:126-136. 10.1016/j.canlet.2008.09.039, 19008039.
70. Jeggo PA, Lobrich M. Artemis links ATM to double strand break rejoining. Cell Cycle 2005, 4:359-362.
71. Huang HY, Hu LL, Song TJ, Li X, He Q, Sun X, Li YM, Lu HJ, Yang PY, Tang QQ. Involvement of cytoskeleton-associated proteins in the commitment of C3H10T1/2 pluripotent stem cells to adipocyte lineage induced by BMP2/4. Mol Cell Proteomics 2010,
72. Allan GJ, Beattie J, Flint DJ. Epithelial injury induces an innate repair mechanism linked to cellular senescence and fibrosis involving IGF-binding protein-5. J Endocrinol 2008, 199:155-164. 10.1677/JOE-08-0269, 18676497.
73. Anderson HC, Reynolds PR, Hsu HH, Missana L, Masuhara K, Moylan PE, Roach HI. Selective synthesis of bone morphogenetic proteins-1, -3, -4 and bone sialoprotein may be important for osteoinduction by Saos-2 cells. J Bone Miner Metab 2002, 20:73-82. 10.1007/s007740200010, 11862528.