The genetics of hydatidiform moles: New lights on an ancient disease

Clinical Genetics

Volumn 71, Issue 1, 2007, Pages 25-34

  Slim, Rima ^a,b   Mehio, A ^a  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MONTREAL GENERAL HOSPITAL   (Canada)

Author keywords

Familial hydatidiform moles; Hydatidiform moles; Inflammation; Molar; NALP7; Pregnancies; recurrent hydatidiform moles; Spontaneous abortions

Indexed keywords

NUCLEOSIDE TRIPHOSPHATASE; PROTEIN NALP7;

APOPTOSIS; CLINICAL FEATURE; CYTOGENETICS; DECIDUALIZATION; EPIGENETICS; FAMILY HISTORY; GENE FUNCTION; GENE LOCUS; GENE MUTATION; HISTOPATHOLOGY; HUMAN; HYDATIDIFORM MOLE; IMMUNOLOGY; IMMUNOPATHOGENESIS; INFLAMMATION; NONHUMAN; OOCYTE DEVELOPMENT; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; TROPHOBLAST;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CHROMOSOMES, HUMAN, PAIR 19; EPIGENESIS, GENETIC; FEMALE; HUMANS; HYDATIDIFORM MOLE; INHERITANCE PATTERNS; MUTATION; PREGNANCY; PROTEIN STRUCTURE, TERTIARY;

EID: 33845543892     PISSN: 00099163     EISSN: 13990004     Source Type: Journal    
DOI: 10.1111/j.1399-0004.2006.00697.x     Document Type: Review

References (89)

1. Smellie W. A collection of cases and observations in midwifery: To illustrate his former treatise, or first volume on that subject. 1768.
2. Brews A. Hydatidiform mole and chorion-epithelioma. J Obstet Gynaecol Br Empire 1939: 46 (5): 813-835.
3. Bonilla-Musoles F. The diagnosis of gestational trophoblastic neoplasm by ultrasonography. In: Chervenak FA, Isaacson GC, Campbell S, eds. Ultrasound in obstetrics and gynecology, Vol. 2. Boston: Little, Brown and Company, 1993: 1665-1673.
4. Bracken MB. Incidence and aetiology of hydatidiform mole: An epidemiological review. Br J Obstet Gynaecol 1987: 94 (12): 1123-1135.
5. Bracken MB, Brinton LA, Hayashi K. Epidemiology of hydatidiform mole and choriocarcinoma. Epidemiol Rev 1984: 6: 52-75.
6. Copeland LJ. Gestational trophoblastic neoplasia. In: Copeland LJ, ed. Textbook of gynecology. Philadelphia: W.B. Saunders Company, 1993: 1133-1151.
7. Grimes DA. Epidemiology of gestational trophoblastic disease. Am J Obstet Gynecol 1984: 150 (3): 309-318.
8. Steigrad SJ. Epidemiology of gestational trophoblastic diseases. Best Pract Res Clin Obstet Gynaecol 2003: 17 (6): 837-847.
9. Craighill MC, Cramer DW. Epidemiology of complete molar pregnancy. J Reprod Med 1984: 29 (11): 784-787.
10. Palmer JR. Advances in the epidemiology of gestational trophoblastic disease. J Reprod Med 1994: 39 (3): 155-162.
11. Matsuura J, Chiu D, Jacobs PA, Szulman AE. Complete hydatidiform mole in Hawaii: An epidemiological study. Genet Epidemiol 1984: 1 (3): 271-284.
12. Tham BW, Everard JE, Tidy JA, Drew D, Hancock BW. Gestational trophoblastic disease in the Asian population of Northern England and North Wales. Br J Obstet Gynaecol 2003: 110 (6): 555-559.
13. Altieri A, Franceschi S, Ferlay J, Smith J, La Vecchia C. Epidemiology and aetiology of gestational trophoblastic diseases. Lancet Oncol 2003: 4 (11): 670-678.
14. Jacobs PA, Hunt PA, Matsuura JS, Wilson CC, Szulman AE. Complete and partial hydatidiform mole in Hawaii: Cytogenetics, morphology and epidemiology. Br J Obstet Gynaecol 1982: 89 (4): 258-266.
15. Javey H, Sajadi H. Hydatidiform mole in southern Iran: A statistical survey of 113 cases. Int J Gynaecol Obstet 1978: 15 (5): 390-395.
16. Mazzanti P, La Vecchia C, Parazzini F, Bolis G. Frequency of hydatidiform mole in Lombardy, Northern Italy. Gynecol Oncol 1986: 24 (3): 337-342.
17. Paradinas FJ, Browne P, Fisher RA, Foskett M, Bagshawe KD, Newlands E. A clinical, histopathological and flow cytometric study of 149 complete moles, 146 partial moles and 107 non-molar hydropic abortions. Histopathology 1996: 28 (2): 101-110.
18. Parazzini F, La Vecchia C, Franceschi S, Mangili G. Familial trophoblastic disease: Case report. Am J Obstet Gynecol 1984: 149 (4): 382-383.
19. Sand PK, Lurain JR, Brewer JI. Repeat gestational trophoblastic disease. Obstet Gynecol 1984: 63 (2): 140-144.
20. Berkowitz RS, Im SS, Bernstein MR, Goldstein DP. Gestational trophoblastic disease. Subsequent pregnancy outcome, including repeat molar pregnancy. J Reprod Med 1998: 43 (1): 81-86.
21. Ambani LM, Vaidya RA, Rao CS, Daftary SD, Motashaw ND. Familial occurrence of trophoblastic disease - report of recurrent molar pregnancies in sisters in three families. Clin Genet 1980: 18 (1): 27-29.
22. La Vecchia C, Franceschi S, Fasoli M, Mangioni C. Gestational trophoblastic neoplasms in homozygous twins. Obstet Gynecol 1982: 60 (2): 250-252.
23. Vejerslev LO, Sunde L, Hansen BF, Larsen JK, Christensen IJ, Larsen G. Hydatidiform mole and fetus with normal karyotype: Support of a separate entity. Obstet Gynecol 1991: 77 (6): 868-874.
24. Kircheisen R, Ried T. Hydatidiform moles. Hum Reprod 1994: 9 (9): 1783-1784.
25. Seoud M, Khalil A, Frangieh A, Zahed L, Azar G, Nuwayri-Salti N. Recurrent molar pregnancies in a family with extensive intermarriage: report of a family and review of the literature. Obstet Gynecol 1995: 86 (4 Pt 2): 692-695.
26. Mazhar S, Janjua S. Recurrent familial hydatidiform mole. J Pakistan Inst Med Sci 1995: 6 (1,2): 383-386.
27. Sensi A, Gualandi F, Pittalis MC et al. Mole maker phenotype: Possible narrowing of the candidate region. Eur J Hum Genet 2000: 8 (8): 641-644.
28. Judson H, Hayward BE, Sheridan E, Bonthron DT. A global disorder of imprinting in the human female germ line. Nature 2002: 416 (6880): 539-542.
29. Fisher RA, Hodges MD, Rees HC et al. The maternally transcribed gene p57(KIP2) (CDNK1C) is abnormally expressed in both androgenetic and biparental complete hydatidiform moles. Hum Mol Genet 2002: 11 (26): 3267-3272.
30. Fallahian M. Familial gestational trophoblastic disease. Placenta 2003: 24 (7): 797-799.
31. Hodges MD, Rees HC, Seckl MJ, Newlands ES, Fisher RA. Genetic refinement and physical mapping of a biparental complete hydatidiform mole locus on chEomosome 19q13.4. J Med Genet 2003: 40 (8): e95.
32. Al-Hussaini TK, Abd el-Aal DM, Van den Veyver IB. Recurrent pregnancy loss due to familial and non-familial habitual molar pregnancy. Int J Gynaecol Obstet 2003: 83 (2): 179-186.
33. Agarwal P, Bagga R, Jain V, Kalra J, Gopalan S. Familial recurrent molar pregnancy: A case report. Acta Obstet Gynecol Scand 2004: 83 (2): 213-214.
34. Zhao J, Moss J, Sebire NJ et al. Analysis of the chromosomal region 19q13.4 in two Chinese families with recurrent hydatidiform mole. Hum Reprod 2006: 21 (2): 536-541.
35. Shih Ie M, Kurman RJ. Molecular basis of gestational trophoblastic diseases. Curr Mol Med 2002: 2 (1): 1-12.
36. Sasaki S. Clinical presentation and management of molar pregnancy. Best Pract Res Clin Obstet Gynaecol 2003: 17 (6): 885-892.
37. Szulman AE, Surti U. The syndromes of hydatidiform mole. II. Morphologic evolution of the complete and partial mole. Am J Obstet Gynecol 1978: 132 (1): 20-27.
38. Zaragoza MV, Keep D, Genest DR, Hassold T, Redline RW. Early complete hydatidiform moles contain inner cell mass derivatives. Am J Med Genet 1997: 70 (3): 273-277.
39. Fukunaga M. Early partial hydatidiform mole: Prevalence, histopathology, DNA ploidy, and persistence rate. Virchows Arch 2000: 437 (2): 180-184.
40. Hertig A, Edmonds H. Genesis of hydatidiform mole. 1940.
41. Minelli E, Buchi C, Granata P et al. Cytogenetic findings in echographically defined blighted ovum abortions. Ann Genet 1993: 36 (2): 107-110.
42. Roesler M, Wise L, Katayama KP. Karyotype analysis of blighted ova in pregnancies achieved by in vitro fertilization. Fertil Steril 1989: 51 (6): 1065-1066.
43. Trabetti E, Galavotti R, Zanini L et al. The parental origin of hydatidiform moles and blighted ova: Molecular probing with hypervariable DNA polymorphisms. Mol Cell Probes 1993: 7 (4): 325-329.
44. Baggish MS, Woodruff JD, Tow SH, Jones HW Jr. Sex chromatin pattern in hydatidiform mole. Am J Obstet Gynecol 1968: 102 (3): 362-370.
45. Kajii T, Ohama K. Androgenetic origin of hydatidiform mole. Nature 1977: 268 (5621): 633-634.
46. Surti U, Szulman AE, O'Brien S. Complete (classic) hydatidiform mole with 46,XY karyotype of paternal origin. Hum Genet 1979: 51 (2): 153-155.
47. Kovacs BW, Shahbahrami B, Tast DE, Curtin JP. Molecular genetic analysis of complete hydatidiform moles. Cancer Genet Cytogenet 1991: 54 (2): 143-152.
48. Lindor NM, Ney JA, Gaffey TA, Jenkins RB, Thibodeau SN, Dewald GW. A genetic review of complete and partial hydatidiform moles and nonmolar triploidy. Mayo Clin Proc 1992: 67 (8): 791-799.
49. Helwani MN, Seoud M, Zahed L, Zaatari G, Khalil A, Slim R. A familial case of recurrent hydatidiform molar pregnancies with biparental genomic contribution. Hum Genet 1999: 105 (1-2): 112-115.
50. Moglabey YB, Kircheisen R, Seoud M, El Mogharbel N, Van den Veyver I, Slim R. Genetic mapping of a maternal locus responsible for familial hydatidiform moles. Hum Mol Genet 1999: 8 (4): 667-671.
51. Panichkul PC, Al-Hussaini TK, Sierra R et al. Recurrent biparental hydatidiform mole: Additional evidence for a 1.1-Mb locus in 19q13.4 and candidate gene analysis. J Soc Gynecol Investig 2005: 12 (5): 376-383.
52. Slim R, Fallahian M, Riviere JB, Zali MR. Evidence of a genetic heterogeneity of familial hydatidiform moles. Placenta 2005: 26 (1): 5-9.
53. Linder D, McCaw BK, Hecht F. Parthenogenic origin of benign ovarian teratomas. N Engl J Med 1975: 292 (2): 63-66.
54. Surani MA, Barton SC, Norris ML. Nuclear transplantation in the mouse: heritable differences between parental genomes after activation of the embryonic genome. Cell 1986: 45 (1): 127-136.
55. Solter D. Differential imprinting and expression of maternal and paternal genomes. Annu Rev Genet 1988: 22: 127-146.
56. Coullin P. [From human andro- and parthenogenesis (hydatidiform moles and benign ovarian teratomas) to cancer]. Gynecol Obstet Fertil 2005: 33 (7-8): 469-482.
57. Wake N, Takagi N, Sasaki M. Androgenesis as a cause of hydatidiform mole. J Natl Cancer Inst 1978: 60 (1): 51-57.
58. Jacobs PA, Wilson CM, Sprenkle JA, Rosenshein NB, Migeon BR. Mechanism of origin of complete hydatidiform moles. Nature 1980: 286 (5774): 714-716.
59. Loukinov DI, Pugacheva E, Vatolin S et al. BORIS, a novel male germ-line-specific protein associated with epigenetic reprogramming events, shares the same 11-zinc-finger domain with CTCF, the insulator protein involved in reading imprinting marks in the soma. Proc Natl Acad Sci USA 2002: 99 (10): 6806-6811.
60. Wolffe AP. Transcriptional control: Imprinting insulation. Curr Biol 2000: 10 (12): R463-R465.
61. Ohlsson R, Renkawitz R, Lobanenkov V. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet 2001: 17 (9): 520-527.
62. Recillas-Targa F, Pikaart MJ, Burgess-Beusse B et al. Position-effect protection and enhancer blocking by the chicken beta-globin insulator are separable activities. Proc Natl Acad Sci USA 2002: 99 (10): 6883-6888.
63. Chao W, Huynh KD, Spencer RJ, Davidow LS, Lee JT. CTCF, a candidate trans-acting factor for X-inactivation choice. Science 2002: 295 (5553): 345-347.
64. El-Maarri O, Seoud M, Coullin P et al. Maternal alleles acquiring paternal methylation patterns in biparental complete hydatidiform moles. Hum Mol Genet 2003: 12 (12): 1405-1413.
65. El-Maarri O, Seoud M, Riviere JB et al. Patients with familial biparental hydatidiform moles have normal methylation at imprinted genes. Eur J Hum Genet 2005: 13 (4): 486-490.
66. Djuric U, El-Maarri O, Lamb B et al. Familial molar tissues due to mutations in the inflammatory gene, NALP7, have normal postzygotic DNA methylation. Human Genetics 2006. DOI:10-1007.S00439-006-0192-3.
67. Medawar PB. Some immunological and endocrinologgical problems raised by the evolution of viviparity in vertebrates. Society for Experimental Biology 1953: Symposia No. 11: 320-338.
68. Halbrecht I, Komlos L. Lymphocyte transformation in mixed wife-husband leukocyte cultures in abortions and in hydatidiform moles. Obstet Gynecol 1968: 31 (2): 173-177.
69. Lauritsen JG, Kristensen T, Grunnet N. Depressed mixed lymphocyte culture reactivity in mothers with recurrent spontaneous abortion. Am J Obstet Gynecol 1976: 125 (1): 35-39.
70. Lewis J Jr, Whang J, Nagel B, Oppenheim JJ, Perry S. Lymphocyte transformation in mixed leukocyte cultures in women with normal pregnancy or tumors of placental origin. A preliminary report. Am J Obstet Gynecol 1966: 96 (2): 287-290.
71. Rocklin RE, Kitzmiller JL, Carpenter CB, Garovoy MR, David JR. Maternal-fetal relation. Absence of an immunologic blocking factor from the serum of women with chronic abortions. N Engl J Med 1976: 295 (22): 1209-1213.
72. Lewis JL Jr, Terasaki PI. HL-A leukocyte antigen studies in women with gestational trophoblastic neoplasms. Am J Obstet Gynecol 1971: 111 (4): 547-554.
73. Couillin P, Afoutou JM, Faye O, Ravise N, Correa P, Boue A. Androgenetic origin of African complete hydatidiform moles demonstrated by HLA markers. Hum Genet 1985: 71 (2): 113-116.
74. Takeuchi S. Immunology of spontaneous abortion and hydatidiform mole. Am J Reprod Immunol 1980: 1 (1): 23-28.
75. Labarrere CA, Althabe OH. Primary chronic abortion, preeclampsia, idiopathic intrauterine growth retardation, hydatidiform mole, and choriocarcinoma: A unifying concept. Am J Reprod Immunol Microbiol 1986: 10 (4): 156-157.
76. Murdoch S, Djuric U, Mazhar B et al. Mutations in NALP7 cause recurrent hydatidiform moles and reproductive wastage in humans. Nat Genet 2006: 38 (3): 300-302.
77. Tschopp J, Martinon F, Burns K. NALPs: A novel protein family involved in inflammation. Nat Rev Mol Cell Biol 2003: 4 (2): 95-104.
78. Okada K, Hirota E, Mizutani Y et al. Oncogenic role of NALP7 in testicular seminomas. Cancer Sci 2004: 95 (12): 949-954.
79. Kinoshita T, Wang Y, Hasegawa M, Imamura R, Suda T. PYPAF3, a PYRIN-containing APAF-1-like protein, is a feedback regulator of caspase-1-dependent interleukin-1{beta} secretion. J Biol Chem 2005: 280 (23): 21720-21725.
80. Bestor TH, Bourc'his D. Genetics and epigenetics of hydatidiform moles. Nat Genet 2006: 38 (3): 274-276.
81. Tong ZB, Gold L, Pfeifer KE et al. Mater, a maternal effect gene required for early embryonic development in mice. Nat Genet 2000: 26 (3): 267-268.
82. Dalbies-Tran R, Papillier P, Pennetier S, Uzbekova S, Monget P. Bovine mater-like NALP9 is an oocyte marker gene. Mol Reprod Dev 2005: 71 (4): 414-421.
83. Horikawa M, Kirkman NJ, Mayo KE et al. The mouse germ-cell-specific leucine-rich repeat protein NALP14: A member of the NACHT nucleoside triphosphatase family. Biol Reprod 2005: 72 (4): 879-889.
84. Strakova Z, Srisuparp S, Fazleabas AT. IL-1beta during in vitro decidualization in primate. J Reprod Immunol 2002: 55 (1-2): 35-47.
85. Karmakar S, Das C. Regulation of trophoblast invasion by IL-1beta and TGF-beta1. Am J Reprod Immunol 2002: 48 (4): 210-219.
86. Chaouat G, Ledee-Bataille N, Zourbas S et al. Cytokines, implantation and early abortion: Re-examining the Th1/Th2 paradigm leads to question the single pathway, single therapy concept. Am J Reprod Immunol 2003: 50 (3): 177-186.
87. Berkowitz RS, Mostoufizadeh GhM, Kabawat SE, Goldstein BP, Driscoll SG. Immunopathologic study of the implantation site in molar pregnancy. Am J Obstet Gynecol 1982: 144 (8): 925-930.
88. Kabawat SE, Mostoufi-Zadeh M, Berkowitz RS, Driscoll SG, Goldstein BP, Bhan AK. Implantation site in complete molar pregnancy: A study of immunologically competent cells with monoclonal antibodies. Am J Obstet Gynecol 1985: 152 (1): 97-99.
89. Wongweragiat S, Searle RF, Bulmer JN. Decidual T lymphocyte activation in hydatidiform mole. J Clin Pathol 1999: 52 (12): 888-894.