Uterine-specific loss of Tsc2 leads to myometrial tumors in both the uterus and lungs

Molecular Endocrinology

Volumn 27, Issue 9, 2013, Pages 1403-1414

  Prizant, Hen ^a   Sen, Aritro ^a   Light, Allison ^a   Cho, Sung Nam ^b   DeMayo, Francesco J ^b   Lydon, John P ^b   Hammes, Stephen R ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; ESTRADIOL; ESTROGEN; LETROZOLE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROGESTERONE; PROTEIN S6; RAPAMYCIN; SEX HORMONE; TUBERIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE DELETION; LUNG; LUNG LYMPHANGIOLEIOMYOMATOSIS; LUNG TUMOR; LYMPHANGIOLEIOMYOMATOSIS; MOUSE; MYOMETRIUM; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR VOLUME; TUMOR XENOGRAFT; UTERINE CELL; UTERUS; UTERUS MYOMA;

ANIMALS; AROMATASE; AROMATASE INHIBITORS; CELL PROLIFERATION; FEMALE; LEIOMYOMA; LUNG NEOPLASMS; MALE; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MYOMETRIUM; ORGAN SPECIFICITY; OVARIECTOMY; SEXUAL MATURATION; SIROLIMUS; TUBEROUS SCLEROSIS; UTERINE NEOPLASMS; UTERUS;

EID: 84883240838     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2013-1059     Document Type: Article

References (70)

1. Zhe X, Schuger L. Combined smooth muscle and melanocytic differentiation in lymphangioleiomyomatosis. J Histochem Cytochem. 2004;52(12):1537-1542.
2. Ferrans VJ, Yu ZX, Nelson WK, et al. Lymphangioleiomyomatosis (LAM): a review of clinical and morphological features. J Nihon Med Sch. 2000;67(5):311-329.
3. Taveira-DaSilva AM, Pacheco-Rodriguez G, Moss J. The natural history of lymphangioleiomyomatosis: markers of severity, rate of progression and prognosis. Lymphat Res Biol. 2010;8(1):9-19.
4. Henske EP, McCormack FX. Lymphangioleiomyomatosis-a wolf in sheep's clothing. J Clin Invest. 2012;122(11):3807-3816.
5. Klarquist J, Barfuss A, Kandala S, et al. Melanoma-associated antigen expression in lymphangioleiomyomatosis renders tumor cells susceptible to cytotoxic T cells. Am J Pathol. 2009;175(6):2463-2472.
6. Dibble CC, Elis W, Menon S, et al. TBC1D7 is a third subunit of the TSC1-TSC2 complex upstream of mTORC1. Mol Cell. 2012;47(4): 535-546.
7. McCormack F, Brody A, Meyer C, et al. Pulmonary cysts consistent with lymphangioleiomyomatosis are common in women with tuberous sclerosis: genetic and radiographic analysis. Chest. 2002; 121(suppl 3):61S.
8. Yu J, Henske EP. mTORactivation, lymphangiogenesis, and estrogenmediated cell survival: the "perfect storm" of pro-metastatic factors in LAM pathogenesis. Lymphat Res Biol. 2010;8(1):43-49.
9. Seyama K, Kumasaka T, Kurihara M, Mitani K, Sato T. Lymphangioleiomyomatosis: a disease involving the lymphatic system. Lymphat Res Biol. 2010;8(1):21-31.
10. Glasgow CG, Taveira-Dasilva AM, Darling TN, Moss J. Lymphatic involvement in lymphangioleiomyomatosis. Ann N Y Acad Sci. 2008;1131:206-214.
11. Astrinidis A, Khare L, Carsillo T, et al. Mutational analysis of the tuberous sclerosis gene TSC2 in patients with pulmonary lymphangioleiomyomatosis. J Med Genet. 2000;37(1):55-57.
12. Karbowniczek M, Astrinidis A, Balsara BR, et al. Recurrent lymphangiomyomatosis after transplantation: genetic analyses reveal a metastatic mechanism. Am J Respir Crit Care Med. 2003;167(7): 976-982.
13. Smolarek TA, Wessner LL, McCormack FX, Mylet JC, Menon AG, Henske EP. Evidence that lymphangiomyomatosis is caused by TSC2 mutations: chromosome 16p13 loss of heterozygosity in angiomyolipomas and lymph nodes from women with lymphangiomyomatosis. Am J Hum Genet. 1998;62(4):810-815.
14. Carsillo T, Astrinidis A, Henske EP. Mutations in the tuberous sclerosis complex gene TSC2 are a cause of sporadic pulmonary lymphangioleiomyomatosis. Proc Natl Acad Sci USA. 2000; 97(11):6085-6090.
15. Sato T, Seyama K, Fujii H, Maruyama H, et al. Mutation analysis of the TSC1 and TSC2 genes in Japanese patients with pulmonary lymphangioleiomyomatosis. J Hum Genet. 2002;47(1):20-28.
16. Oh YM, Mo EK, Jang SH, et al. Pulmonary lymphangioleiomyomatosis in Korea. Thorax. 1999;54(7):618-621.
17. Johnson SR, Tattersfield AE. Clinical experience of lymphangioleiomyomatosis in the UK. Thorax. 2000;55(12):1052-1057.
18. Kitaichi M, Nishimura K, Itoh H, Izumi T. Pulmonary lymphangioleiomyomatosis: a report of 46 patients including a clinicopathologic study of prognostic factors. Am J Respir Crit Care Med. 1995;151(2, Pt 1):527-533.
19. Yu JJ, Robb VA, Morrison TA, et al. Estrogen promotes the survival and pulmonary metastasis of tuberin-null cells. Proc Natl Acad Sci USA. 2009;106(8):2635-2640.
20. Glassberg MK, Elliot SJ, Fritz J, et al. Activation of the estrogen receptor contributes to the progression of pulmonary lymphangioleiomyomatosis via matrix metalloproteinase-induced cell invasiveness. J Clin Endocrinol Metab. 2008;93(5):1625-1633.
21. Taveira-DaSilva AM, Stylianou MP, Hedin CJ, Hathaway O, Moss J. Decline in lung function in patients with lymphangioleiomyomatosis treated with or without progesterone. Chest. 2004;126(6):1867-1874.
22. Johnson SR, Tattersfield AE. Decline in lung function in lymphangioleiomyomatosis: relation to menopause and progesterone treatment. Am J Respir Crit Care Med. 1999;160(2):628-633.
23. Adamson D, Heinrichs WL, Raybin DM, Raffin TA. Successful treatment of pulmonary lymphangiomyomatosis with oophorectomy and progesterone. Am Rev Respir Dis. 1985;132(4):916-921.
24. Khalife WI, Mahmoud F, Larson E, Hardie R. Pulmonary lymphangioleiomyomatosis in a postmenopausal woman: case report with review of literature. S D J Med. 2005;58(4):139-143.
25. Hayashi T, Kumasaka T, Mitani K, et al. Prevalence of uterine and adnexal involvement in pulmonary lymphangioleiomyomatosis: a clinicopathologic study of 10 patients. Am J Surg Pathol. 2011; 35(12):1776-1785.
26. Tietze L, Günther K, Hörbe A, et al. Benign metastasizing leiomyoma: a cytogenetically balanced but clonal disease. Hum Pathol. 2000;31(1):126-128.
27. Bowen JM, Cates JM, Kash S, et al. Genomic imbalances in benign metastasizing leiomyoma: characterization by conventional karyotypic, fluorescence in situ hybridization, and whole genome SNP array analysis. Cancer Genet. 2012;205(5):249-254.
28. Goyle KK, Moore DF Jr, Garrett C, Goyle V. Benign metastasizing leiomyomatosis: case report and review. Am J Clin Oncol. 2003; 26(5):473-476.
29. Awonuga AO, Shavell VI, Imudia AN, Rotas M, Diamond MP, Puscheck EE. Pathogenesis of benign metastasizing leiomyoma: a review. Obstet Gynecol Surv. 2010;65(3):189-195.
30. Hernandez O, Way S, McKenna J 3rd, Gambello MJ. Generation of a conditional disruption of the Tsc2 gene. Genesis. 2007;45(2): 101-106.
31. Soyal SM, Mukherjee A, Lee KY, et al. Cre-mediated recombination in cell lineages that express the progesterone receptor. Genesis. 2005;41(2):58-66.
32. Daikoku T, Hirota Y, Tranguch S, et al. Conditional loss of uterine Pten unfailingly and rapidly induces endometrial cancer in mice. Cancer Res. 2008;68(14):5619-5627.
33. Kim TH, Franco HL, Jung SY, et al. The synergistic effect of Mig-6 and Pten ablation on endometrial cancer development and progression. Oncogene. 2010;29(26):3770-3780.
34. Lee L, Sudentas P, Donohue B, et al. Efficacy of a rapamycin analog (CCI-779) and IFN-gamma in tuberous sclerosis mouse models. Genes Chromosomes Cancer. 2005;42(3):213-227.
35. Kenerson H, Dundon TA, Yeung RS. Effects of rapamycin in the Eker rat model of tuberous sclerosis complex. Pediatr Res. 2005; 57(1):67-75.
36. Maruo T, Ohara N, Wang J, Matsuo H. Sex steroidal regulation of uterine leiomyoma growth and apoptosis. Hum Reprod Update. 2004;10(3):207-220.
37. Benassayag C, Leroy MJ, Rigourd V, et al. Estrogen receptors (ERα/ ERβ) in normal and pathological growth of the human myometrium: pregnancy and leiomyoma. Am J Physiol. 1999;276(6, Pt 1): E1112-1118.
38. Fuchs-Young R, Howe S, Hale L, Miles R, Walker C. Inhibition of estrogen-stimulated growth of uterine leiomyomas by selective estrogen receptor modulators. Mol Carcinog. 1996;17(3):151-159.
39. Gakhar G, Wight-Carter M, Andrews G, Olson S, Nguyen TA. Hydronephrosis and urine retention in estrogen-implanted athymic nude mice. Vet Pathol. 2009;46(3):505-508.
40. Leavitt WW, Takeda A. Hormonal regulation of estrogen and progestin receptors in decidual cells. Biol Reprod. 1986;35(2):475-484.
41. Taveira-DaSilva AM, Hathaway O, Stylianou M, Moss J. Changes in lung function and chylous effusions in patients with lymphangioleiomyomatosis treated with sirolimus. Ann Intern Med. 2011; 154(12):797-805, W-292-293.
42. Malhowski AJ, Hira H, Bashiruddin S, et al. Smooth muscle protein-22-mediated deletion of Tsc1 results in cardiac hypertrophy that is mTORC1-mediated and reversed by rapamycin. Hum Mol Genet. 2011;20(7):1290-1305.
43. McCormack FX, Inoue Y, Moss J, et al. Efficacy and safety of sirolimus in lymphangioleiomyomatosis. N Engl J Med. 2011; 364(17):1595-1606.
44. Bissler JJ, McCormack FX, Young LR, et al. Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis. New Engl J Med. 2008;358(2):140-151.
45. Taillé C, Borie R, Crestani B. Current management of lymphangioleiomyomatosis. Curr Opin Pulm Med. 2011;17(5):374-378.
46. Yu J, Parkhitko AA, Henske EP. Mammalian target of rapamycin signaling and autophagy: roles in lymphangioleiomyomatosis therapy. Proc Am Thorac Soc. 2010;7(1):48-53.
47. Kinder B, McCormack FX. Clinical trials for rare lung diseases: lessons from lymphangioleiomyomatosis. Lymphat Res Biol. 2010; 8(1):71-79.
48. Walker CL. Role of hormonal and reproductive factors in the etiology and treatment of uterine leiomyoma. Recent Prog Horm Res. 2002;57:277-294.
49. Evans P, Brunsell S. Uterine fibroid tumors: diagnosis and treatment. Am Fam Physician. 2007;75(10):1503-1508.
50. Glasgow CG, Steagall WK, Taveira-Dasilva A, et al. Lymphangioleiomyomatosis (LAM): molecular insights lead to targeted therapies. Respir Med. 2010;104(suppl 1):S45-S58.
51. Matsui K, Takeda K, Yu ZX, et al. Downregulation of estrogen and progesterone receptors in the abnormal smooth muscle cells in pulmonary lymphangioleiomyomatosis following therapy. An immunohistochemical study. Am J Respir Crit Care Med. 2000;161(3, Pt 1): 1002-1009.
52. Wahedna I, Cooper S, Williams J, Paterson IC, Britton JR, Tattersfield AE. Relation of pulmonary lymphangio-leiomyomatosis to use of the oral contraceptive pill and fertility in the UK: a national case control study. Thorax. 1994;49(9):910-914.
53. Brunelli A, Catalini G, Fianchini A. Pregnancy exacerbating unsus pected mediastinal lymphangioleiomyomatosis and chylothorax. Int J Gynaecol Obstet. 1996;52(3):289-290.
54. Cohen MM, Freyer AM, Johnson SR. Pregnancy experiences among women with lymphangioleiomyomatosis. Respir Med. 2009;103(5):766-772.
55. Yu J, Astrinidis A, Howard S, Henske EP. Estradiol and tamoxifen stimulate LAM-associated angiomyolipoma cell growth and activate both genomic and nongenomic signaling pathways. Am J Physiol Lung Cell Mol Physiol. 2004;286(4):L694-L700.
56. Marino M, Galluzzo P, Ascenzi P. Estrogen signaling multiple pathways to impact gene transcription. Curr Genomics. 2006;7(8):497-508.
57. Hoekstra AV, Sefton EC, Berry E, et al. Progestins activate the AKT pathway in leiomyoma cells and promote survival. J Clin Endocrinol Metab. 2009;94(5):1768-1774.
58. Ishikawa H, Ishi K, Serna VA, Kakazu R, Bulun SE, Kurita T. Progesterone is essential for maintenance and growth of uterine leiomyoma. Endocrinology. 2010;151(6):2433-2442.
59. Sawicka EH, Morris AJ. A report of two long-surviving cases of pulmonary lymphangioleiomyomatosis and the response to progesterone therapy. Br J Dis Chest. 1985;79(4):400-406.
60. Poh SC, Wang YT. Lymphangioleiomyomatosis-treatment with progesterone. Singapore Med J. 1991;32(4):258-261.
61. Bittmann I, Rolf B, Amann G, Löhrs U. Recurrence of lymphangioleiomyomatosis after single lung transplantation: new insights into pathogenesis. Hum Pathol. 2003;34(1):95-98.
62. Rege AS, Snyder JA, Scott WJ. Benign metastasizing leiomyoma: a rare cause of multiple pulmonary nodules. Ann Thorac Surg. 2012; 93(6):e149-e151.
63. Goto T, Maeshima A, Akanabe K, et al. Benign metastasizing leiomyoma of the lung. Ann Thorac Cardiovasc Surg. 2012;18(2):121-124.
64. Walker CL, Hunter D, Everitt JI. Uterine leiomyoma in the Eker rat: a unique model for important diseases of women. Genes Chromosomes Cancer. 2003;38(4):349-356.
65. Kwiatkowski DJ. Animal models of lymphangioleiomyomatosis (LAM) and tuberous sclerosis complex (TSC). Lymphat Res Biol. 2010;8(1):51-57.
66. Kwiatkowski DJ, Zhang H, Bandura JL, et al. A mouse model of TSC1 reveals sex-dependent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tsc1 null cells. Hum Mol Genet. 2002;11(5):525-534.
67. Kobayashi T, Minowa O, Sugitani Y, et al. A germ-line Tsc1 mutation causes tumor development and embryonic lethality that are similar, but not identical to, those caused by Tsc2 mutation in mice. Proc Natl Acad Sci USA. 2001;98(15):8762-8767.
68. Onda H, Lueck A, Marks PW, Warren HB, Kwiatkowski DJ. Tsc2(α/β) mice develop tumors in multiple sites that express gelsolin and are influenced by genetic background. J Clin Invest. 1999; 104(6):687-695.
69. Liu F, Lunsford EP, Tong J, et al. Real-time monitoring of tumorigenesis, dissemination, drug response in a preclinical model of lymphangioleiomyomatosis/tuberous sclerosis complex. PloS one. 2012;7(6):e38589.
70. Goncharova EA, Goncharov DA, Fehrenbach M, et al. Prevention of alveolar destruction and airspace enlargement in a mouse model of pulmonary lymphangioleiomyomatosis (LAM). Sci Transl Med. 2012;4(154):154ra134.