Sex steroidal targets & genetic susceptibility to idiopathic cryptorchidism

Pediatric Endocrinology Reviews

Volumn 6, Issue 4, 2009, Pages 481-490

  Massart, Francesco ^a   Saggese, Giuseppe ^a  

^a Department of Pediatrics   (Italy)

Author keywords

Cryptorchidism, androgen receptor; Estrogen receptor; Gene; Mutation; Polymorphism; Steroidogenic factor 1; Testicular dysgenesis syndrome

Indexed keywords

ANDROGEN RECEPTOR; ENDOCRINE DISRUPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; STEROIDOGENIC FACTOR 1;

CRYPTORCHISM; DISEASE PREDISPOSITION; ENVIRONMENTAL EXPOSURE; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC SUSCEPTIBILITY; HUMAN; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; REVIEW; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; TESTIS DESCENT;

ANIMALS; CRYPTORCHIDISM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC PREDISPOSITION TO DISEASE; GONADAL STEROID HORMONES; HUMANS; MALE; MODELS, BIOLOGICAL; RECEPTORS, ANDROGEN; RECEPTORS, ESTROGEN; STEROIDOGENIC FACTOR 1;

EID: 67650797240     PISSN: 15654753     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (100)

1. Boisen KA, Kaleva M, Main KM, Virtanen HE, Haavisto AM, Schmidt IM, Chellakooty M, Damgaard IN, Mau C, Reunanen M, Skakkebaek NE, Toppari J. Difference in prevalence of congenital cryptorchidism in infants between two Nordic countries. Lancet 2004;363:1264-1269 (Pubitemid 38496487)
2. Foresta C, Zuccarello D, Garolla A, Ferlin A. Role of hormones, genes and environment in human cryptorchidism. Endocr Rev 2008;29:560-580
3. Virtanen HE, Toppari J. Epidemiology and pathogenesis of cryptorchidism. Hum Reprod Update 2008;14:49-58
4. Toppari J, Kaleva M, Virtanen HE. Trends in the incidence of cryptorchidism and hypospadias, and methodological limitations of registry-based data. Hum Reprod Update 2001;7:282-286 (Pubitemid 32451651)
5. Adami HO, Bergström R, Möhner M, Zatonski W, Storm H, Ekbom A, Tretli S, Teppo L, Ziegler H, Rahu M, Gurevicius R, Stengerevics A. Testicular cancer in nine northern European countries. Int J Cancer 1994;59:33-38 (Pubitemid 2140078)
6. Huyghe E, Matsuda T, Thonneau P. Increasing incidence of testicular cancer worldwide: a review. J Urol 2003;170:5-11 (Pubitemid 36734401)
7. Carlsen E, Giwercman A, Keiding N, Skakkebæk NE. Evidence for decreasing quality of semen during past 50 years. BMJ 1992;305:609-613
8. Jouannet P, Wang C, Eustache F, Kold-Jensen T, Auger J. Semen quality and male reproductive health: the controversy about human sperm concentration decline. APMIS 2001;109:333-344 (Pubitemid 32651695)
9. Skakkebæk NE, Rajpert-De Meyts E, Main KM. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 2001;16:972-978 (Pubitemid 32451837)
10. Sharpe RM, Skakkebæk NE. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract? Lancet 1993;341:1392-1395
11. Aschim EL, Giwercman A, Ståhl O, Eberhard J, Cwikiel M, Nordenskjöld A, Haugen TB, Grotmol T, Giwercman YL. The Rsal polymorphism in the estrogen receptor-beta gene is associated with male infertility. J Clin Endocrinol Metab 2005;90:5343-5348 (Pubitemid 41262299)
12. Levy JB, Husmann DA. The hormonal control of testicular descent. J Androl 1995;16:459-463
13. Hutson JM, Hasthorpe S, Heyns CF. Anatomical and functional aspects of testicular descent and cryptorchidism. Endocrinol Rev 1997;18:259-280 (Pubitemid 27171523)
14. Van der Schoot P, Emmen JMA. Development, structure, and function of the cranial suspensory ligaments of the mammalian gonads in a cross-species perspective; their possible role in effecting disturbed testicular descent. Hum Reprod Update 1996;2:399-418
15. Heyns CF, Hutson JM. Historical review of theories on testicular descent. J Urol 1995;153:754-767
16. Lubahn DB, Joseph DR, Sullivan PM, Willard HF, French FS, Wilson EM. Cloning of human androgen receptor complementary DNA and localization to the X chromosome. Science 1988;240:327-330 (Pubitemid 18116696)
17. Quigley CA, De Bellis A, Marschke KB, el-Awady MK, Wilson EM, French FS. Androgen receptor defects: historical, clinical, and molecular perspectives. Endocrine Reviews 1995;16:271-321
18. Galani A, Kitsiou-Tzeli S, Sofokleous C, Kanavakis E, Kalpini-Mavrou A. Androgen insensitivity syndrome: clinical features and molecular defects. Hormones 2008;7:217-229
19. McPhaul MJ, Marcelli M, Zoppi S, Wilson CM, Griffin JE, Wilson JD. Mutations in the ligand-binding domain of the androgen receptor gene cluster in two regions of the gene. J Clin Invest 1992;90:2097-2101
20. McPhaul MJ, Marcelli M, Zoppi S, Griffin JE, Wilson JD. Genetic basis of endocrine disease. The spectrum of mutations in the androgen receptor gene that causes androgen resistance. J Clin Endocrinol Metab 1993;76:17-23 (Pubitemid 23027545)
21. Zoppi S, Marcelli JP, Griffin JE, Deslypere JP, Wilson JD, McPhaul MJ. Amino acid substitutions in the DNA binding domain of the human androgen receptor are a frequent cause of receptor binding positive androgen resistance. Mol Endocrinol 1992;6:409-415
22. Brinkmann AO. Molecular basis of androgen insensitivity. Mol Cell Endocrinol 2001;179:105-109
23. Sultan C, Paris F, Terouanne B, Balaguer P, Georget V, Poujol N, Jeandel C, Lumbroso S, Nicolas JC. Disorders linked to insufficient androgen action in male children. Hum Reprod Update 2001;7:314-322 (Pubitemid 32440293)
24. Ferlin A, Vinanzi C, Garolla A, Selice R, Zuccarello D, Cazzadore C, Foresta C. Male infertility and androgen receptor gene mutations: clinical features and identification of seven novel mutations. Clin Endocrinol (Oxf) 2006;65:606-610 (Pubitemid 44583820)
25. Boehmer AL, Brinkmann O, Bruggenwirth H, van Assendelft C, Otten BJ, Verleun-Mooijman MC, Niermeijer MF, Brunner HG, Rouwe' CW, Waelkens JJ, Oostdijk W, Kleijer WJ, van der Kwast TH, de Vroede MA, Drop SL. Genotype versus phenotype in families with androgen insensitivity syndrome. J Clin Endocrinol Metab 2001;86:4151-4160 (Pubitemid 32848528)
26. Barthold JS, Kumasi-Rivers K, Upadhyay J, Shekarriz B, Imperato-Mcginley J. Testicular position in the androgen insensitivity syndrome: implications for the role of androgens in testicular descent. J Urol 2000;164:497-501 (Pubitemid 30481974)
27. Wiener JS, Marcelli M, Gonzales Jr ET, Roth DR, Lamb DJ. Androgen receptor gene alterations are not associated with isolated cryptorchidism. J Urol 1998;160:863-865 (Pubitemid 29479545)
28. Suzuki Y, Sasagawa I, Ashida J, Nakada T, Muroya K, Ogata T. Screening for mutations of the androgen receptor gene in patients with isolated cryptorchidism. Fertil Steril 2001;76:834-836 (Pubitemid 32928416)
29. Palazzolo I, Gliozzi A, Rusmini P, Sau D, Crippa V, Simonini F, Onesto E, Bolzoni E, Poletti A. The role of the polyglutamine tract in androgen receptor. J Steroid Biochem Mol Biol 2008;108:245-253 (Pubitemid 351187919)
30. Choong CS, Wilson EM. Trinucleotide repeats in the human androgen receptor: a molecular basis for disease. J Mol Endocrinol 1998;21:235-257 (Pubitemid 29005397)
31. Gao T, Marcelli M, McPhaul MJ. Transcriptional activation and transient expression of the human androgen receptor. J Steroid Biochem Mol Biol 1996;59:9-20 (Pubitemid 27014137)
32. Aschim EL, Nordenskjöld A, Giwercman A, Lundin KB, Ruhayel Y, Haugen TB, Grotmol T, Giwercman YL. Linkage between cryptorchidism, hypospadias, and GGN repeat length in the androgen receptor gene. J Clin Endocrinol Metab 2004;89:5105-5109 (Pubitemid 39391456)
33. Radpour R, Rezaee M, Tavasoly A, Solati S, Saleki A. Association of long polyglycine tracts (GGN repeats) in exon 1 of the androgen receptor gene with cryptorchidism and penile hypospadias in Iranian patients. J Androl 2007;28:164-169 (Pubitemid 46048090)
34. Ferlin A, Garolla A, Bettella A, Bartoloni L, Vinanzi C, Roverato A, Foresta C. Androgen receptor gene CAG and GGC repeat lengths in cryptorchidism. Eur J Endocrinol 2005;152:419-425 (Pubitemid 40439495)
35. La Spada AR, Wilson EM, Lubahn DB, Harding AE, Fischbeck KH. Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature (Lond) 1991;352:77-79
36. Tut TG, Ghadessy FJ, Trifiro MA, Pinsky L, Yong EL. Long polyglutamine tracts in the androgen receptor are associated with reduced transactivation, impaired sperm production, and male infertility. J Clin Endocrinol Metab 1997;82:3777-3782 (Pubitemid 27509371)
37. Ogata T, Muroya K, Ishii T, Suzuki Y, Nakada T, Sasagawa I. Undermasculinized genitalia in a boy with an abnormally expanded CAG repeat length in the androgen receptor gene. Clin Endocrinol 2001;54:835-838 (Pubitemid 34208895)
38. Lim HN, Chen H, McBride S, Dunning AM, Nixon RM, Hughes IA, Hawkins JR. Longer polyglutamine tracts in the androgen receptor are associated with moderate to severe undermasculinized genitalia in XY males. Hum Mol Genet 2000;9:829-834 (Pubitemid 30162768)
39. Lim HN, Nixon RM, Chen H, Hughes IA, Hawkins JR. Evidence that longer androgen receptor polyglutamine repeats are a causal factor for genital abnormalities. J Clin Endocrinol Metab 2001;86:3207-3210 (Pubitemid 32673489)
40. Sasagawa I, Suzuki Y, Tateno T, Nakada T, Muroya K, Ogata T. CAG repeat length of the androgen receptor gene in Japanese males with cryptorchidism. Mol Hum Reprod 2000;6:973-975 (Pubitemid 30947674)
41. Silva-Ramos M, Oliveira JM, Cabeda JM, Reis A, Soares J, Pimenta A. The CAG repeat within the androgen receptor gene and its relationship to cryptorchidism. Int Braz J Urol 2006;32:330-335 (Pubitemid 44056880)
42. Sartor O, Zheng Q, Eastham JA. Androgen receptor gene CAG repeat length varies in a race-specific fashion in men without prostate cancer. Urology 1999;53:378-380 (Pubitemid 29063330)
43. Irvine RA, Yu MC, Ross RK, Coetzee GA. The CAG and GGC microsatellites of the androgen receptor gene are in linkage disequilibrium in men with prostate cancer. Cancer Res 1995;55:1937-1940
44. Edwards A, Hammond HA, Jin L, Caskey CT, Chakraborty R. Genetic variation at five trimeric and tetrameric tandem repeat loci in four human population groups. Genomics 1992;12:241-253
45. Hsing AW, Gao YT, Wu G, Wang X, Deng J, Chen YL, Sesterhenn IA, Mostofi FK, Benichou J, Chang C. Polymorphic CAG and GGN repeat lengths in the androgen receptor gene and prostate cancer risk: a population-based case-control study in China. Cancer Res 2000;60:5111-5116 (Pubitemid 30739768)
46. Berkowitz GS, Lapinski RH. Risk factors for cryptorchidism: a nested case-control study. Paediatr Perinat Epidemiol 1996;10:39-51 (Pubitemid 26014350)
47. Ferlin A, Bartoloni L, Rizzo G, Roverato A, Garolla A, Foresta C. Androgen receptor gene CAG and GGC repeat lengths in idiopathic male infertility. Molecular Human Reproduction 2004;10:417-421 (Pubitemid 38714374)
48. Mhatre AN, Trifiro MA, Kaufman M, Kazemi-Esfarjani P, Figlewicz D, Rouleau G, Pinsky L. Reduced transcriptional regulatory competence of the androgen receptor in X-linked spinal and bulbar muscular atrophy. Nat Genet 1993;5:184-188 (Pubitemid 23293456)
49. Kazemi-Esfarjani P, Trifiro MA, Pinsky L. Evidence for a repressive function of the long polyglutamine tract in the human androgen receptor: possible pathogenetic relevance for the (CAG)n-expanded neuronopathies. Hum Mol Genet 1995;4:523-527
50. He B, Wilson EM. The NH(2)-terminal and carboxyl-terminal interaction in the human androgen receptor. Mol Genet Metab 2002;75:293-298
51. Poletti A. The polyglutamine tract of androgen receptor: from functions to dysfunctions in motor neurons. Front Neuroendocrinol 2004;25:1-26 (Pubitemid 38744538)
52. Toppari J, Larsen JC, Christiansen P, Giwercman A, Grandjean P, Guillette LJ Jr, Jégou B, Jensen TK, Jouannet P, Keiding N, Leffers H, McLachlan JA, Meyer O, Müller J, Rajpert-De Meyts E, Scheike T, Sharpe R, Sumpter J, Skakkebaek NE. Male reproductive health and environmental xenoestrogens. Environ Health Perspect 1996;104:741-803 (Pubitemid 26290302)
53. Sharpe RM. The 'oestrogen hypothesis' - where do we stand now? Int J Androl 2003;6:2-15
54. Ivell R, Hartung S. The molecular basis of cryptorchidism. Mol Hum Reprod 2003;9:175-181
55. Nef S, Shipman T, Parada LF. A molecular basis for estrogen-induced cryptorchidism. Dev Biol 2000;224:354-361
56. Emmen JM, McLuskey A, Adham IM, Engel W, Verhoef-Post M, Themmen AP, Grootegoed JA, Brinkmann AO. Involvement of insulin-like factor 3 (Insl3) in diethylstilbestrol-induced cryptorchidism. Endocrinology 2000;141:846-849 (Pubitemid 32250510)
57. McLachlan JA. Environmental signaling: what embryos and evolution teach us about endocrine disrupting chemicals. Endocr Rev 2001;22:319-341
58. Smith EP, Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, Williams TC, Lubahn DB, Korach KS. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med 1994;331:1056-1061 (Pubitemid 24317698)
59. O'Donnell L, Robertson KM, Jones ME, Simpson ER. Estrogen and spermatogenesis. Endocr Rev 2001;22:289-318
60. Donaldson KM, Tong SY, Washburn T, Lubahn DB, Eddy EM, Hutson JM, Korach KS. Morphometric study of the gubernaculum in male estrogen receptor mutant mice. J Androl 1996;17:91-95 (Pubitemid 26131751)
61. Gennari L, Becherini L, Falchetti A, Masi L, Massart F, Brandi ML. Genetics of osteoporosis: role of steroid hormone receptor gene polymorphisms. J Steroid Biochem Mol Biol 2002; 81:1-24 (Pubitemid 34785919)
62. McGuire WL, Chamness GC, Fuqua SW. Abnormal estrogen receptor in clinical breast cancer. J Steroid Biochem Mol Biol 1992;43:243-247
63. Zhang Q-X, Borg A, Fuqua SAW. An exon 5 deletion variant of the estrogen receptor frequently coexpressed with wild-type estrogen receptor in human breast cancer. Cancer Res 1993;53:5882-5884 (Pubitemid 24006154)
64. Yoshida R, Fukami M, Sasagawa I, Hasegawa T, Kamatani N, Ogata T. Association of cryptorchidism with a specific haplotype of the estrogen receptor α gene: implication for the susceptibility to estrogenic environmental endocrine disruptors. J Clin Endocrinol Metab 2005;90:4716-4721 (Pubitemid 41159363)
65. Galan JJ, Guarducci E, Nuti F, Gonzalez A, Ruiz M, Ruiz A, Krausz C. Molecular analysis of estrogen receptor α gene AGATA haplotype and SNP12 in European populations: potential protective effect for cryptorchidism and lack of association with male infertility. Hum Reprod 2007;22:444-449 (Pubitemid 46152566)
66. Heimdal K, Andersen TI, Skrede M, Fosså SD, Berg K, Børresen AL. Association studies of estrogen receptor polymorphisms in a Norwegian testicular cancer population. Cancer Epidemiol Biomarkers Prev 1995;4:123-126
67. Wang Y, Barthold J, Figueroa E, González R, Noh PH, Wang M, Manson J. Analysis of five single nucleotide polymorphisms in the ESR1 gene in cryptorchidism. Birth Defects Res A Clin Mol Teratol 2008;82:482-485 (Pubitemid 351928453)
68. Kukuvitis A, Georgiou I, Bouba I, Tsirka A, Giannouli CH, Yapijakis C, Tarlatzis B, Bontis J, Lolis D, Sofikitis N, Papadimas J. Association of oestrogen receptor alpha polymorphisms and androgen receptor CAG trinucleotide repeats with male infertility: a study in 109 Greek infertile men. Int J Androl 2002;25:149-152 (Pubitemid 34595740)
69. Suzuki Y, Sasagawa I, Itoh K, Ashida J, Muroya K and Ogata T. Estrogen receptor alpha gene polymorphism is associated with idiopathic azoospermia. Fertil Steril 2002;78:1341-1343 (Pubitemid 35463143)
70. Galan JJ, Buch B, Cruz N, Segura A, Moron FJ, Bassas L, Martinez-Pineiro L, Real LM, Ruiz A. Multilocus analyses of estrogen-related genes reveal involvement of the ESR1 gene in male infertility and the polygenic nature of the pathology. Fertil Steril 2005;84:910-918 (Pubitemid 41414580)
71. Guarducci E, Nuti F, Becherini L, Rotondi M, Balercia G, Forti G and Krausz C. Estrogen receptor alpha promoter polymorphism: stronger estrogen action is coupled with lower sperm count. Hum Reprod 2006;21:994-1001
72. Becherini L, Gennari L, Masi L, Mansani R, Massart F, Morelli A, Falchetti A, Gonnelli S, Fiorelli G, Tanini A, Brandi ML. Evidence of a linkage disequilibrium between polymorphisms in the human estrogen receptor alpha gene and their relationship to bone mass variation in postmenopausal Italian women. Hum Mol Genet 2000;9:2043-2050 (Pubitemid 30642669)
73. Terwilliger JD, Ott J. Handbook of Human Genetic Linkage. Baltimore: Johns Hopkins University Press 1994
74. Davidson S. Research suggests importance of haplotypes over SNPs. Nat Biotechnol 2000;18:1134-1135
75. Agoulnik AI. Cryptorchidism - an estrogen spoil? J Clin Endocrinol Metab 2005;90:4975-4977
76. Johnson JM, Edwards S, Shoemaker D, Schadt EE. Dark matter in the genome: evidence of widespread transcription detected by microarray tiling experiments. Trends Genet 2005;21:93-102 (Pubitemid 40127353)
77. Gingerich TJ, Feige JJ, LaMarre J. AU-rich elements and the control of gene expression through regulated mRNA stability. Anim Health Res Rev 2004;5:49-63
78. Rosenkranz K, Hinney A, Ziegler A, Hermann H, Fichter M, Mayer H, Siegfried W, Young JK, Remschmidt H, Hebebrand J. Systematic mutation screening of the estrogen receptor β gene in probands of different weight extremes: identification of several genetic variants. J Clin Endocrinol Metab 1998;83:4524-4527 (Pubitemid 29100162)
79. Gennari L, Merlotti D, De Paola V, Calabrò A, Becherini L, Martini G, Nuti R. Estrogen receptor gene polymorphisms and the genetics of osteoporosis: a HuGE review. Am J Epidemiol 2005;161:307-320 (Pubitemid 40256202)
80. Sundarrajan C, Liao WX, Roy AC, Ng SC. Association between estrogen receptor-β gene polymorphisms and ovulatory dysfunctions in patients with menstrual disorders. J Clin Endocrinol Metab 2001;86:135-139 (Pubitemid 32109786)
81. Försti A, Zhao C, Israelsson E, Dahlman-Wright K, Gustafsson JA, Hemminki K. Polymorphisms in the estrogen receptor β gene and risk of breast cancer: no association. Breast Cancer Res Treat 2003;79:409-413 (Pubitemid 36750948)
82. Ogawa S, Inoue S, Watanabe T, Orimo A, Hosoi T, Ouchi Y, Muramatsu M. Molecular cloning and characterization of human estrogen receptor βcx: a potential inhibitor of estrogen action in human. Nucleic Acids Res 1998;26:3505-3512 (Pubitemid 28347221)
83. Peng B, Lu B, Leygue E, Murphy LC. Putative functional characteristics of human estrogen receptor-β isoforms. J Mol Endocrinol 2003;30:13-29 (Pubitemid 36305253)
84. Shen LX, Basilion JP, Stanton Jr VP. Single-nucleotide polymorphisms can cause different structural folds of mRNA. Proc Natl Acad Sci USA 1999;96:7871-7876
85. Iida K, Akashi H. A test of translational selection at 'silent' sites in the human genome: base composition comparisons in alternatively spliced genes. Gene 2000;261:93-105
86. Parker KL, Schimmer BP. Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr Rev 1997;18:361-377 (Pubitemid 27246881)
87. Zimmermann S, Schwarzler A, Buth S, Engel W, Adham IM. Transcription. of the Leydig insulin-like gene is mediated by steroidogenic factor-1. Mol Endocrinol 1998;12:706-713 (Pubitemid 30659072)
88. Adham IM, Agoulnik AI. Insulin-like 3 signalling in testicular descent. Int J Androl 2004;27:257-265
89. Krylova IN, Sablin EP, Moore J, Xu RX, Waitt GM, MacKay JA, Juzumiene D, Bynum JM, Madauss K, Montana V, Lebedeva L, Suzawa M, Williams JD, Williams SP, Guy RK, Thornton JW, Fletterick RJ, Willson TM, Ingraham HA. Structural analyses reveal phosphatidyl inositols as ligands for the NR5 orphan receptors SF-1 and LRH-1. Cell 2005;120:343-355 (Pubitemid 40222429)
90. Li Y, Choi M, Cavey G, Daugherty J, Suino K, Kovach A, Bingham NC, Kliewer SA, Xu HE. Crystallographic identification and functional characterization of phospholipids as ligands for the orphan nuclear receptor steroidogenic factor-1. Mol Cell 2005;17:491-502 (Pubitemid 40269114)
91. WuQiang F, Yanase T, Wei L, Oba K, Nomura M, Okabe T, Goto K, Nawata H. Functional characterization of a new human Ad4BP/SF-1 variation, G146A. Biochem Biophys Res Commun 2003;311:987-994 (Pubitemid 37393416)
92. Wada Y, Okada M, Fukami M, Sasagawa I, Ogata T. Association of cryptorchidism with Gly146Ala polymorphism in the gene for steroidogenic factor-1. Fertil Steril 2006;85:787-790 (Pubitemid 43261589)
93. Ferlin A, Simonato M, Bartoloni L, Rizzo G, Bettella A, Dottorini T, Dallapiccola B, Foresta C. The INSL3-LGR8/GREAT ligand-receptor pair in human cryptorchidism. J Clin Endocrinol Metab 2003;88:4273-4279 (Pubitemid 37153731)
94. Hasegawa T, Fukami M, Sato N, Katsumata N, Sasaki G, Fukutani K, Morohashi K, Ogata T. Testicular dysgenesis without adrenal insufficiency in a 46,XY patient with a heterozygous inactive mutation of steroidogenic factor-1. J Clin Endocrinol Metab 2004;89:5930-5935 (Pubitemid 39628395)
95. Ito M, Achermann JC, Jameson JL. A naturally occurring steroidogenic factor-1 mutation exhibits differential binding and activation of target genes. J Biol Chem 2000;275:31708-31714 (Pubitemid 30782048)
96. Bodmer WF. The HLA-system. In: Albert ED, Baur MP, Mayr WR (eds), Histocompatibility Testing, Berlin. Springer 1984;pp. 11-22
97. Greenberg, DA. Linkage analysis of "necessary" disease loci versus "susceptibility" loci. Am J Hum Genet 1993;48:135-143
98. Massart F, Marcucci G, ML Brandi ML. Pharmacogenetics of bone treatments: the VDR and ERα gene story. Pharmacogenomics 2008;9:733-746
99. Massart F. Human races and pharmacogenomics in bone effective treatments. Gynecol Endocrinol 2005:20:36-44 (Pubitemid 40445239)
100. Massart F, Reginster JY, Brandi ML. Genetics of menopause-associated diseases. Maturitas 2001;40(2):103-116