HMGI(Y) and HMGI-C dysregulation: A common occurrence in human tumors

Advances in Anatomic Pathology

Volumn 6, Issue 5, 1999, Pages 237-246

  Tallini, Giovanni ^a   Dal Cin, Paola ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

High mobility group proteins; HMGI(Y); HMGI C; Lipoma; Mesenchymal tumor genetics; Molecular genetics; Uterine leiomyoma

Indexed keywords

HIGH MOBILITY GROUP A1A PROTEIN; HIGH MOBILITY GROUP A2 PROTEIN; HIGH MOBILITY GROUP PROTEIN; TRANSCRIPTION FACTOR; TUMOR PROTEIN;

FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LEIOMYOMA; LIPOMA; METABOLISM; NEOPLASM; REVIEW; UTERUS CANCER;

FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HIGH MOBILITY GROUP PROTEINS; HMGA1A PROTEIN; HMGA2 PROTEIN; HUMANS; LEIOMYOMA; LIPOMA; NEOPLASM PROTEINS; NEOPLASMS; TRANSCRIPTION FACTORS; UTERINE NEOPLASMS;

EID: 0033192556     PISSN: 10724109     EISSN: 15334031     Source Type: Journal    
DOI: 10.1097/00125480-199909000-00001     Document Type: Review

References (94)

1. Bustin M. High mobility group chromosomal proteins: architectural components that facilitate chromatin function. Prog Nucl Acid Res Mol Biol 1996;54:35-100.
2. Goodwin GH, Johns EW. Isolation and characterisation of two calf thymus chromatin non-histone proteins with high contents of acidic and basic aminoacids. Eur J Biochem 1973;3:215-9.
3. Grosschedl R, Giese K, Pagel J. HMG domain proteins: architectural elements in the assembly of nucleoprotein structures. TIG 1994;10:94-100. (Pubitemid 24075089)
4. Lovell-Badge R. Living with bad architecture. Nature 1995;376:725-6.
5. Bustin M, Lehn DA, Landsman D. Structural features of the HMG chromosomal proteins and their genes. Biochim Biophys Acta 1990;1049:231-43. (Pubitemid 20224615)
6. Yamazaki F, Nagatsuka Y, Shirakawa H, Yoshida M. Repression of cell cycle progression by antisense HMG2 RNA. Biochem Biophys Res Commun 1995;210:1045-51.
7. Bruhn S, Pil PM, Essigmann JM, Housman DE, Lippard SJ. Isolation and characterization of human cDNA clones encoding a high mobility group box protein that recognizes structural distortions to DNA caused by binding of the anticancer agent cisplatin. Proc Natl Acad Sci USA 1992;89:2307-11.
8. Huang JC, Zamble DB, Reardon JT, Lippard SJ, Sancar A. HMG-domain proteins specifically inhibit the repair of the major DNA adduct of the anticancer drug cysplatinum by human excision nuclease. Proc Natl Acad Sci USA 1994;91:10394-8. (Pubitemid 24329003)
9. Treiber DK, Zhai X, Jantzen HM, Essigman JM. Cysplatin-DNA adducts are molecular decoys for the ribosomal RNA transcription factor HUBF (human upstream binding factor). Proc Natl Acad Sci USA 1994;91:5672-6. (Pubitemid 24174390)
10. Böttger M, Vogel F, Platzer M, Kiessling U, Grade K, Strauss M. Condensation of vector DNA by the chromosomal protein HMGI results in efficient transfection. Biochem Biophys Acta 1988;950:221-8.
11. Sandig V, Stamm W, Behlke J, Böttger M, Strauss M. Direct gene transfer of HMG1 based DNA-protein complexes [Abstract]. J Mol Med 1995;73:B10.
12. Bustin M, Alfonso PJ, Pash JM, Ward JM, Gearhart JD, Reeves RH. Characterization of transgenic mice with an increased content of chromosomal protein HMG-14 in their chromatin. DNA Cell Biol 1995;14:997-1005. (Pubitemid 26002056)
13. Giancotti V, Bandiera A, Ciani L, et al. High-mobility-group (HMG) proteins and histone H1 subtypes expression in normal and tumor tissues of mouse. Eur J Biochem 1993;213:825-32. (Pubitemid 23125654)
14. Reeves R. Chromatin changes during the cell cycle. Curr Opin Cell Biol 1992;4:413-23.
15. Radic MZ, Saghbini M, Elton TS, Reeves R, Hamkalo BA. Hoechst 33258 distamycin A, and high mobility group protein I (HMG-I) compete for binding to mouse satellite DNA. Chromosoma 1992;101:602-8.
16. Disney JE, Johnson KR, Magnuson NS, Sylvester SR, Reeves R. High mobility group protein HMG-I localizes to G/Q- and C-bands of human and mouse chromosomes. J Cell Biol 1989;109:1975-82. (Pubitemid 19282587)
17. Saitoh Y, Laemmli UK. Metaphase chromosome structure: bands arise from a differential folding path of the highly AT-rich scaffold. Cell 1994;76:609-22. (Pubitemid 24070647)
18. Meijer L, Ostvold AC, Walass SI, Lund T, Laland SG. High-mobility-group proteins P1, I and Y as substractes of the M-phase-specific p34cdc2/cyclincdc13 kinase. Eur J Biochem 1991;196:557-67.
19. Johnson KR, Lehn DA, Reeves R. Alternative processing of mRNAs encoding mammalian chromosomal high-mobility-group proteins HMG-I and HMG-Y. Mol Cell Biol 1989;9:2114-23. (Pubitemid 19117812)
20. Patel UA, Bandiera A, Manfioletti G, Giancotti V, Chau K-Y, Crane-Robinson C. Expression and cDNA cloning of human HMGI-C phosphoprotein. Biochem Biophys Res Comm 1994;201:63-70. (Pubitemid 24213694)
21. Friedmann M, Holth LT, Zoghbi HY, Reeves R. Organization, inducible-expression and chromosome localization of the human HMG-I(Y) nonhistone protein gene. Nucleic Acids Res 1993;21:4259-67. (Pubitemid 23279015)
22. Chau K-Y, Patel UA, Lee K-LD, Lam H-YP, Crane-Robinson C. The gene for the human architectural transcription factor HMGI-C consists of five exons each coding for a distinct functional element. Nucleic Acids Res 1995;23:4262-6.
23. Ashar HR, Cherath L, Przybysz KM, Chada K. Genomic characterization of human HMGIC, a member of the accessory transcription factor family found at tranlocation breakpoints in lipomas. Genomics 1996;31:207-14. (Pubitemid 26044776)
24. Kazmierczak B, Bullerdiek J, Hue Pham K, Bartnitzke S, Wiesner H. Intron 3 of HMGIC is the most frequent target of chromosomal aberrations in human tumors and has been conserved basically for at least 30 million years. Cancer Genet Cytogenet 1998;103:175-7. (Pubitemid 128712627)
25. Hirning-Folz U, Wilda M, Rippe V, Bullerdiek J, Hameister H. The expression pattern of the Hmgic gene during development. Genes Chromosomes Cancer 1998;23:350-7. (Pubitemid 28507375)
26. Chiappetta G, Avantaggiato V, Visconti R, et al. High level expression of the HMGI (Y) gene during embryonic development. Oncogene 1996;13:2439-46. (Pubitemid 27026027)
27. Manfioletti G, Giancotti V, Bandiera A, et al. cDNA cloning of the HMGI-C phosphoprotein, a nuclear protein associated with neoplastic and undifferentiated phenotypes. Nucleic Acids Res 1991;19:6793-7. (Pubitemid 21913116)
28. Rogalla P, Drechsler K, Frey G, et al. HMGI-C expression patterns in human tissues. Implications for the genesis of frequent mesenchymal tumors. Am J Pathol 1996;149:775-9. (Pubitemid 26334162)
29. Ogram SA, Reeves R. Differential regulation of a multipromoler gene. Selective 12-0-tetradecanoylphorbol-13-acetate induction of a single transcription start site in the HMG-I/Y gene. J Biol Chem 1995;270:14235-42.
30. Lanahan A, Williams JB, Sanders LK, Nathans D. Growth factor-induced delayed early response genes. Mol Cell Biol 1992;12:3919-29.
31. Xiang X, Benson KF, Chada K. Mini-mouse: disruption of the pygmy locus in a transgenic insertional mutant. Science 1990;247:967-9.
32. Zhou S, Benson KF, Ashar HR. Chada K. Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature 1995;376:771-4.
33. Ruyter-Spira CP, de Groof AJ, van der Poel JJ, et al. The HMGI-C gene is a likely candidate for the autosomal dwarf locus in the chicken. J Hered 1998;89:295-300. (Pubitemid 28366921)
34. Lund T, Holtlund J, Fredricksen M, Laland SG. On the presence of two new high mobility group like proteins in HeLa S3 cells. FEBS Lett 1983;152:163-7. (Pubitemid 13129686)
35. Bussemakers MJG, van de Ven WJM, Debruyne FMJ, Schalken JA. Identification of high mobility group protein I (Y) as potential progression marker for prostate cancer by differential hybridization analysis. Cancer Res 1991;51:606-11.
36. Ram TG, Reeves R, Hosick HL. Elevated high mobility group I(Y) gene expression is associated with progressive transformation of mouse mammary epithelial cells. Cancer Res 1993;53:2655-60. (Pubitemid 23168036)
37. Berlingieri MT, Manfioletti G, Santoro M, et al. Inhibition of HMGI-C protein synthesis suppresses retrovirally induced neoplastic transformation of rat thyroid cells. Mol Cell Biol 1995;15:1545-53.
38. Giancotti V, Pani B, D'Andrea P, et al. Elevated levels of a specific class of nuclear phosphoroproteins in cells transformed with ras and v-mos oncogenes and by co-transfection with c-myc and polyoma middle T genes. EMBO J 1987;6:1981-7.
39. Giancotti V, Buratti E, Perissin L, et al. Analysis of the HMGI nuclear proteins in mouse neoplastic cells induced by different procedures. Exp Cell Res 1989;184:538-45. (Pubitemid 19259736)
40. Tamimi Y, van der Poel HG, Denyn M-M, et al. Increased expression of high mobility group protein I (Y) in high grade prostatic cancer determined by in situ hybridization. Cancer Res 1993;53:5512-6. (Pubitemid 23342176)
41. Fedele M, Bandiera A, Chiappetta G, et al. Human colorectal carcinomas express high levels of high mobility group HMGI(Y) proteins. Cancer Res 1996;56:1896-1901. (Pubitemid 26118229)
42. Chiappetta G, Bandiera A, Berlingieri MT, et al. The expression of the high mobility group HMGI (Y) proteins correlates with the malignant phenotype of human thyroid neoplasms. Oncogene 1995;10:1307-14.
43. Chiappetta G, Tallini G, DeBiasio MC, et al. Detection of high mobility group I HMGI(Y) protein in the diagnosis of thyroid tumors: HMGI(Y) expression represents a potential diagnostic indicator of carcinoma. Cancer Res 1998;58:4193-8. (Pubitemid 28440579)
44. Bandiera A, Bonifacio D, Manfioletti G, et al. Expression of HMGI(Y) proteins in squamous intraepithelial and invasive lesions of the uterine cervix. Cancer Res 1998;58:426-31. (Pubitemid 28087401)
45. Rogalla P, Drechsler K, Kazmierczak B, Rippe V, Bonk U, Bullerdiek J. Expression of HMGI-C a member of the high mobility group protein family, in a subset of breast cancers: relationship to histologic grade. Mol Carcinogen 1997;19:153-6. (Pubitemid 27360132)
46. Rommel B, Rogalla P, Jox A, et al. HMGI-C, a member of the high mobility group family of proteins is expressed in hematopoietic stam cells and leukemic cells. Leuk Lymphoma 1997;26:603-7. (Pubitemid 27477785)
47. Rogalla P, Drechsler K, Schroder-Babo W, Eberhardt K, Bullerdiek J. HMGI-C expression pattern in non-small lung cancer and surrounding tissue. Anticancer Research 1998;18:3327-30. (Pubitemid 28546455)
48. Schoenmakers EFPM, Wanschura S, Mols R, Bullerdiek J, Van den Berghe H, Van de Ven WJM. Recurrent rearrangements in the high mobility group protein gene, HMGI-C, in benign mesenchymal tumours. Nature Genet 1995;10:436-44.
49. Ashar HR, Schoenberg Fejzo M, Tkachenko A, et al. Disruption of the architectural factor HMGI-C: DNA-binding AT hook motifs fused in lipomas to distinct transcriptional regulatory domains. Cell 1995;82:57-65.
50. Mitelman F, ed. Catalog of chromosome aberrations in cancer, 6. New York: John Wiley & Sons, 1998.
51. Schoenmakers EFPM, Kools PFJ, Mols F, et al. Physical mapping of chromosome 12q breakpoints in lipoma, pleomorphic salivary gland adenoma, uterine leiomyoma, and myxoid liposarcoma. Genomics 1994;20:210-22. (Pubitemid 24108398)
52. Wanschura S, Kazmierczak B, Schoenmakers EFPM, et al. Regional fine mapping of the multiple aberration region involved in uterine leiomyomas, lipomas and pleomorphic adenomas of the salivary gland to 12q15. Genes Chromosomes Cancer 1995;14:68-70.
53. Kazmierczak B, Pohnke Y, Bullerdiek J. Fusion transcripts between the HMGI-C gene and RTVLH-related sequences in mesenchymal tumors without cytogenetic aberrations. Genomics 1996;38:223-6. (Pubitemid 26424602)
54. Petit MMR, Mols R, Schoenmakers EFPM, Mandahl N, Van De Ven WJM. LPP, the preferred fusion partner gene of HMGIC in lipomas, is a novel member of the LIM protein gene family. Genomics 1996;36:118-29. (Pubitemid 26277765)
55. Petit MMR, Swarts S, Bridge JA, Van de Ven WJM. Expression of reciprocal fusion transcripts of the HMGIC and LPP genes in parosteal lipoma. Cancer Genet Cytogenet 1998;106:18-23. (Pubitemid 28483427)
56. Rogalla P, Kazmierczak B, Meyer-Bolte K, Tran KH, Bullerdiek J. The t(3;12) (q27;q14-q15) with underlying HMGIC-LPP fusion is not determining an adipocytic phenotype. Genes Chromosomes Cancer 1998;22:100-4. (Pubitemid 28208801)
57. Kazmierczak B, Hennig Y, Wanschura S, et al. Description of a novel fusion transcript between HMGI-C, a gene encoding for a member of the high mobility group proteins, and the mitochondrial aldehyde dehydrogenase gene. Cancer Res 1995;55:6038-9.
58. Geurts JMW, Schoenmakers EFPM, Roijer E, Stenman G, Van de Ven WJM. Expression of reciprocal hybrid transcripts of HMGIC and FHIT in a pleomorphic adenoma of the parotid gland. Cancer Res 1997;57:13-7. (Pubitemid 27020320)
59. Geurts JMW, Schoenmakers EFPM, Roijer E, Astrom A-K, Stenman G, Van de Ven WJM. Identification of NFIB as recurrent translocation partner gene of HMGIC in pleomorphic adenomas. Oncogene 1998;16:865-72. (Pubitemid 28102589)
60. Kazmierczak B, Rosigkeit J, Wanschura S, et al. HMGI-C rearrangements as the molecular basis for the majority of pulmonary chondroid hamartomas: a survey of 30 tumors. Oncogene 1996;12:515-21. (Pubitemid 26059645)
61. Kazmierczak B, Dal Cin P, Wanschura S, Bartnitzke S, Van den Berghe H, Bullerdiek J. Cloning and molecular characterization of part of a new gene fused to HMGIC in mesenchymal tumors. Am J Pathol 1998;152:431-5. (Pubitemid 28106389)
62. Dal Cin P, Timmerman D, Van den Berghe I, et al. Genomic changes in endometrial polyps associated with tamoxifen show no evidence for its action as an external carcinogen. Cancer Res 1998;58:2278-81. (Pubitemid 28252678)
63. Staats B, Bonk U, Wanschura S, et al. A fibroadenoma with a t(4:12) (q27;q15) affecting the HMGI-C gene, a member of the high mobility group protein gene family. Breast Cancer Res Treat 1996;38:299-308.
64. Rohen C, Caselitz J, Stern C, et al. A hamartoma of the breast with an aberration of 12q mapped to the MAR region by fluorescence in situ hybridization. Cancer Genet Cytogenet 1995;84:82-4.
65. Wanschura S, Kazmierczak B, Pohnke Y, et al. Transcriptional activation of HMGI-C in three pulmonary hamartomas each with a der(14) t(12:14) as the sole cytogenetic abnormality. Cancer Letters 1996;102:17-21. (Pubitemid 26097799)
66. Schoenberg Fejzo M, Ashar HR, Krauter KS, et al. Translocation breakpoints upstream of the HMGIC gene in uterine leiomyomata suggest dysregulation of this gene by a mechanism different from that in lipomas. Genes Chromosomes Cancer 1996;17:1-6. (Pubitemid 26327929)
67. Holt JT, Morton CC, Nienhuis AW, Leder P. Molecular mechanisms of hematological neoplasms. In: Stamatoyannopoulos G, Niehuis AW, Leder P, Majenis PW, eds. The molecular basis of blood diseases. Philadelphia: WB Saunders, 1987:360-2.
68. Swerdlow SH, Zukerberg LR, Yang WI et al. The morphologic spectrum of non-Hodgkin's lymphomas with BCLI/cyclin DI gene rearrangements. Am J Surg Pathol 1996;20:627-40. (Pubitemid 26129450)
69. Kazmierczak B, Wanschura S, Meyer-Bolte K, et al. Cytogenetic and molecular analysis of an aggressive angiomyxoma. Am J Pathol 1995;147:580-5.
70. Kazmierczak B, Dal Cin P, Sciot R, Van den Berghe H, Bullerdiek J. Inflammatory myofibroblastic tumor with HMGIC rearrangement. Cancer Genet Cytogenet [in press].
71. Rosai J, Akerman M, Dal Cin P, et al. Combined morphologic and karyotypic study of 59 atypical lipomatous tumors. Evaluation of their relationship and differential diagnosis with other adipose tissue tumors (A report of the CHAMP Study Group). Am J Surg Pathol 1996;20:1182-9. (Pubitemid 26336841)
72. Tallini G, Dal Cin P, Rhoden KR, et al. Expression of HMGI-C and HMGI(Y) in ordinary lipoma and atypical lipomatous tumors. Immunohistochemical reactivity correlates with karyotypic alterations. Am J Pathol 1997;151:37-43.
73. Berner J-M, Meza-Zepeda L, Kools PFJ, et al. HMGIC, the gene for an architectural transcription factor, is amplified and rearranged in a subset of human sarcomas. Oncogene 1997;14:2935-41. (Pubitemid 27315662)
74. Dal Cin P, Wanschura S, Kazmierczak B, et al. Amplification and expression of the HMGIC gene in a benign endometrial polyp. Genes Chromosomes Cancer 1998;22:95-9. (Pubitemid 28208800)
75. Kools PFJ, Van de Ven WJM. Amplication of rearranged form of the high mobility group protein gene HMGIC in OsA-C1 osteosarcoma cells. Cancer Genet Cytogenet 1997;91:1-7. (Pubitemid 26398357)
76. Kazmierczak B, Wanschura S, Rommel B, Bartnitzke S, Bullerdiek J. Ten pulmonary chondroid hamartomas with chromosome 6p21 breakpoints within the HMG-I(Y) gene or its immediate surroundings. J Natl Cancer Inst 1996;88:1234-6. (Pubitemid 26302038)
77. Xiao S, Lux ML, Reeves R, Hudson TJ, Fletcher JA. HMGI(Y) activation by chromosome 6p21 rearrangements in multilineage mesenchymal cells from pulmonary hamartoma. Am J Pathol 1997;150:901-10. (Pubitemid 27106162)
78. Tkachenko A, Ashar HR, Meloni AM, Sandberg AA, Chada KK. Misexpression of discrupted HMGI architectural factors activates alternative pathways of tumorigenesis. Cancer Res 1997;57:2276-80. (Pubitemid 27247049)
79. Williams AJ, Powell WL, Collins T, Morton CC. HMGI(Y) expression in human uterine leiomyomata. Involvement of another high-mobility group architectural factor in a benign neoplasm. Am J Pathol 1997;150:911-8. (Pubitemid 27106163)
80. Kazmierczak B, Dal Cin P, Wanschura S, et al. HMGIY is the target of 6p21.3 rearrangements in various benign mesenchymal tumors. Genes Chromosomes Cancer 1998;23:279-85. (Pubitemid 28507366)
81. Dal Cin P, Wanschura S, Christiaens M-R, et al. Hamartoma of the breast with involvement of 6p21 and rearrangement of HMGIY. Genes Chromosomes Cancer 1997;20:90-2. (Pubitemid 27377104)
82. Dal Cin P, Fusco A, Beige G, et al. Involvement of the HMGI(Y) gene in a microfollicualr adenoma of the thyroid. Genes Chromosomes Cancer 1999;24:286-9. (Pubitemid 29070170)
83. Wanschura S, Dal Cin P, Kazmierczak B, Barnitze S, Van den Berghe H, Bullerdiek J. Hidden paracentric inversions of chromosome arm 12q affecting the HMGI-C gene. Genes Chromosomes Cancer 1997;18:322-3. (Pubitemid 27161405)
84. Fedele M, Berlingieri MT, Scala S, et al. Truncated and chimeric HMGI-C genes induce neoplastic transformation of NIH3T3 murine fibroblasts. Oncogene 1998;17:413-8. (Pubitemid 28395904)
85. Mashal RD, Schoenberg Fejzo ML, Friedman AJ, et al. Analysis of androgen receptor DNA reveals the independent clonal origin of uterine leiomyomata and the secondary nature of cytogenetic aberrations in the development of leiomyomata. Genes Chromosomes Cancer 1994;11:1-6. (Pubitemid 24273967)
86. Broberg K, Hoglung M, Limon J, et al. Rearrangement of the neoplasia-associated gene HMGIC in synovia from patients with osteoarthritis. Genes Chromosomes Cancer 1999;24:278-82. (Pubitemid 29070168)
87. Fletcher JA, Pinkus GS, Weidner N, et al. Lineage-restricted clonality in biphasic solid tumors. Am J Pathol 1991;138:1199-1207.
88. Fletcher JA, Pinkus GS, Donavan K, et al. Clonal rearrangement of band 6p21 in the mesenchymal component of pulmonary chondroid hamartoma. Cancer Res 1992;52:6224-8.
89. Fletcher JA, Pinkus JL, Lage JM, et al. Clonal 6p2l rearrangement is restricted to the mesenchymal component of an endometrial polyp. Genes Chromosomes Cancer 1992;5:260-3.
90. Berner J-M, Forus A, Elkahloun A, Meltzer PS, Fodstad í. Myklebost O. Separate amplified regions encompassing CDK4 and MDM2 in human sarcomas. Genes Chromosomes Cancer 1996;17:254-9. (Pubitemid 26424003)
91. Mandahl N, Akerman M, Aman P, et al. Duplication of chromosome segment 12q15-24 is associated with atypical lipomatous tumors: a report of the champ collaborative study group. Int J Cancer 1996;67:632-5. (Pubitemid 26300978)
92. Werner MH, Gronenborn AM, Clore GM. Intercalation, DNA kinking, and the control of transcription. Science 1996;271:778-84. (Pubitemid 26058927)
93. Henderson D and Hurley LH. Molecular struggle for transcriptional control. Nat Med 1995;1:525-7.
94. Farnet CM, Bushman FD. HIV-1 cDNA intergration: requirement of HMGI (Y) protein for function of preintegration complexes in vitro. Cell 1997;88:483-92. (Pubitemid 27154413)