Association between the luteinizing hormone/chorionic gonadotropin receptor (LHCGR) rs4073366 polymorphism and ovarian hyperstimulation syndrome during controlled ovarian hyperstimulation

Reproductive Biology and Endocrinology

Volumn 11, Issue 1, 2013, Pages

  O'Brien, Travis J ^a   Kalmin, Mariah M ^b   Harralson, Arthur F ^c   Clark, Adam M ^a   Gindoff, Ian ^a   Simmens, Samuel J ^b   Frankfurter, David ^a   Gindoff, Paul ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

^c SHENANDOAH UNIVERSITY   (United States)

Author keywords

LHCGR; LHR; OHSS; Ovarian hyperstimulation syndrome; Ovarian stimulation; Polymorphism

Indexed keywords

CHORIONIC GONADOTROPIN; ESTRADIOL; FOLLITROPIN; LUTEINIZING HORMONE CHORIONIC GONADOTROPIN RECEPTOR; LUTEINIZING HORMONE RECEPTOR; THYROTROPIN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; EXON; FEMALE; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC RISK; HAPLOTYPE; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRON; MAJOR CLINICAL STUDY; OVARY FOLLICLE; OVARY HYPERSTIMULATION; PROSPECTIVE STUDY; SINGLE NUCLEOTIDE POLYMORPHISM; AGING; GENETIC POLYMORPHISM; GENETICS; OVARIAN HYPERSTIMULATION SYNDROME; OVULATION INDUCTION; PHYSIOLOGY; PROCEDURES;

ADULT; AGING; FEMALE; GENE FREQUENCY; HUMANS; LINKAGE DISEQUILIBRIUM; OVARIAN HYPERSTIMULATION SYNDROME; OVULATION INDUCTION; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; PROSPECTIVE STUDIES; RECEPTORS, LH;

EID: 84880875328     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-11-71     Document Type: Article

References (70)

1. Scott RT, Toner JP, Muasher SJ, Oehninger S, Robinson S, Rosenwaks Z. Follicle-stimulating hormone levels on cycle day 3 are predictive of in vitro fertilization outcome. Fertil Steril 1989, 51:651-654.
2. Licciardi FL, Liu HC, Rosenwaks Z. Day 3 estradiol serum concentrations as prognosticators of ovarian stimulation response and pregnancy outcome in patients undergoing in vitro fertilization. Fertil Steril 1995, 64:991-994.
3. Ficicioglu C, Kutlu T, Baglam E, Bakacak Z. Early follicular antimullerian hormone as an indicator of ovarian reserve. Fertil Steril 2006, 85:592-596. 10.1016/j.fertnstert.2005.09.019, 16500324.
4. Hsu A, Arny M, Knee AB, Bell C, Cook E, Novak AL, Grow DR. Antral follicle count in clinical practice: analyzing clinical relevance. Fertil Steril 2011, 95:474-479. 10.1016/j.fertnstert.2010.03.023, 20434151.
5. Alviggi C, Humaidan P, Ezcurra D. Hormonal, functional and genetic biomarkers in controlled ovarian stimulation: tools for matching patients and protocols. Reprod Biol Endocrinol 2012, 10:9. 10.1186/1477-7827-10-9, 3299595, 22309877.
6. Altmae S, Hovatta O, Stavreus-Evers A, Salumets A. Genetic predictors of controlled ovarian hyperstimulation: where do we stand today?. Hum Reprod Update 2011, 17:813-828. 10.1093/humupd/dmr034, 21862569.
7. Anagnostou E, Mavrogianni D, Theofanakis C, Drakakis P, Bletsa R, Demirol A, Gurgan T, Antsaklis A, Loutradis D. ESR1, ESR2 and FSH receptor gene polymorphisms in combination: a useful genetic tool for the prediction of poor responders. Curr Pharm Biotechnol 2012, 13:426-434. 10.2174/138920112799361891, 21658000.
8. Boudjenah R, Molina-Gomes D, Torre A, Bergere M, Bailly M, Boitrelle F, Taieb S, Wainer R, Benahmed M, De Mazancourt P, et al. Genetic polymorphisms influence the ovarian response to rFSH stimulation in patients undergoing in vitro fertilization programs with ICSI. PLoS One 2012, 7:e38700. 10.1371/journal.pone.0038700, 3372493, 22701696.
9. Daelemans C, Smits G, De Maertelaer V, Costagliola S, Englert Y, Vassart G, Delbaere A. Prediction of severity of symptoms in iatrogenic ovarian hyperstimulation syndrome by follicle-stimulating hormone receptor Ser680Asn polymorphism. J Clin Endocrinol Metab 2004, 89:6310-6315. 10.1210/jc.2004-1044, 15579795.
10. De Castro F, Moron FJ, Montoro L, Galan JJ, Hernandez DP, Padilla ES, Ramirez-Lorca R, Real LM, Ruiz A. Human controlled ovarian hyperstimulation outcome is a polygenic trait. Pharmacogenetics 2004, 14:285-293. 10.1097/00008571-200405000-00003, 15115914.
11. Desai SS, Achrekar SK, Pathak BR, Desai SK, Mangoli VS, Mangoli RV, Mahale SD. Follicle-stimulating hormone receptor polymorphism (G-29A) is associated with altered level of receptor expression in Granulosa cells. J Clin Endocrinol Metab 2011, 96:2805-2812. 10.1210/jc.2011-1064, 21752882.
12. Jun JK, Yoon JS, Ku SY, Choi YM, Hwang KR, Park SY, Lee GH, Lee WD, Kim SH, Kim JG, Moon SY. Follicle-stimulating hormone receptor gene polymorphism and ovarian responses to controlled ovarian hyperstimulation for IVF-ET. J Hum Genet 2006, 51:665-670. 10.1007/s10038-006-0005-5, 16871362.
13. Loutradis D, Patsoula E, Minas V, Koussidis GA, Antsaklis A, Michalas S, Makrigiannakis A. FSH receptor gene polymorphisms have a role for different ovarian response to stimulation in patients entering IVF/ICSI-ET programs. J Assist Reprod Genet 2006, 23:177-184. 10.1007/s10815-005-9015-z, 3454958, 16758348.
14. Lussiana C, Guani B, Mari C, Restagno G, Massobrio M, Revelli A. Mutations and polymorphisms of the FSH receptor (FSHR) gene: clinical implications in female fecundity and molecular biology of FSHR protein and gene. Obstet Gynecol Surv 2008, 63:785-795. 10.1097/OGX.0b013e31818957eb, 19017414.
15. Sheikhha MH, Eftekhar M, Kalantar SM. Investigating the association between polymorphism of follicle-stimulating hormone receptor gene and ovarian response in controlled ovarian hyperstimulation. J Hum Reprod Sci 2011, 4:86-90. 10.4103/0974-1208.86089, 3205539, 22064672.
16. Wunsch A, Ahda Y, Banaz-Yasar F, Sonntag B, Nieschlag E, Simoni M, Gromoll J. Single-nucleotide polymorphisms in the promoter region influence the expression of the human follicle-stimulating hormone receptor. Fertil Steril 2005, 84:446-453. 10.1016/j.fertnstert.2005.02.031, 16084888.
17. Wunsch A, Sonntag B, Simoni M. Polymorphism of the FSH receptor and ovarian response to FSH. Ann Endocrinol (Paris) 2007, 68:160-166.
18. Altmae S, Haller K, Peters M, Hovatta O, Stavreus-Evers A, Karro H, Metspalu A, Salumets A. Allelic estrogen receptor 1 (ESR1) gene variants predict the outcome of ovarian stimulation in in vitro fertilization. Mol Hum Reprod 2007, 13:521-526. 10.1093/molehr/gam035, 17540666.
19. Georgiou I, Konstantelli M, Syrrou M, Messinis IE, Lolis DE. Oestrogen receptor gene polymorphisms and ovarian stimulation for in-vitro fertilization. Hum Reprod 1997, 12:1430-1433. 10.1093/humrep/12.7.1430, 9262271.
20. Loutradis D, Theofanakis C, Anagnostou E, Mavrogianni D, Partsinevelos GA. Genetic profile of SNP(s) and ovulation induction. Curr Pharm Biotechnol 2012, 13:417-425. 10.2174/138920112799361954, 21657995.
21. Altmae S, Haller K, Peters M, Saare M, Hovatta O, Stavreus-Evers A, Velthut A, Karro H, Metspalu A, Salumets A. Aromatase gene (CYP19A1) variants, female infertility and ovarian stimulation outcome: a preliminary report. Reprod Biomed Online 2009, 18:651-657. 10.1016/S1472-6483(10)60009-0, 19549443.
22. Wang TT, Wu YT, Dong MY, Sheng JZ, Leung PC, Huang HF. G546A polymorphism of growth differentiation factor-9 contributes to the poor outcome of ovarian stimulation in women with diminished ovarian reserve. Fertil Steril 2010, 94:2490-2492. 10.1016/j.fertnstert.2010.03.070, 20451184.
23. Hanevik HI, Hilmarsen HT, Skjelbred CF, Tanbo T, Kahn JA. A single nucleotide polymorphism in BMP15 is associated with high response to ovarian stimulation. Reprod Biomed Online 2011, 23:97-104. 10.1016/j.rbmo.2011.02.015, 21565556.
24. Hillier SG. Gonadotropic control of ovarian follicular growth and development. Mol Cell Endocrinol 2001, 179:39-46. 10.1016/S0303-7207(01)00469-5, 11420129.
25. Webb R, Nicholas B, Gong JG, Campbell BK, Gutierrez CG, Garverick HA, Armstrong DG. Mechanisms regulating follicular development and selection of the dominant follicle. Reprod Suppl 2003, 61:71-90.
26. Ziecik AJ, Kaczmarek MM, Blitek A, Kowalczyk AE, Li X, Rahman NA. Novel biological and possible applicable roles of LH/hCG receptor. Mol Cell Endocrinol 2007, 269:51-60. 10.1016/j.mce.2006.08.016, 17367919.
27. Ziecik AJ, Derecka-Reszka K, Rzucidlo SJ. Extragonadal gonadotropin receptors, their distribution and function. J Physiol Pharmacol 1992, 43:33-49.
28. Ziecik AJ, Derecka K, Gawronska B, Stepien A, Bodek G. Nongonadal LH/hCG receptors in pig: functional importance and parallels to human. Semin Reprod Med 2001, 19:19-30. 10.1055/s-2001-13907, 11394200.
29. Gawronska B, Paukku T, Huhtaniemi I, Wasowicz G, Ziecik AJ. Oestrogen-dependent expression of LH/hCG receptors in pig Fallopian tube and their role in relaxation of the oviduct. J Reprod Fertil 1999, 115:293-301. 10.1530/jrf.0.1150293, 10434935.
30. Perrier d'Hauterive S, Berndt S, Tsampalas M, Charlet-Renard C, Dubois M, Bourgain C, Hazout A, Foidart JM, Geenen V. Dialogue between blastocyst hCG and endometrial LH/hCG receptor: which role in implantation?. Gynecol Obstet Invest 2007, 64:156-160. 10.1159/000101740, 17934312.
31. Hearn MT, Gomme PT. Molecular architecture and biorecognition processes of the cystine knot protein superfamily: part I. The glycoprotein hormones. J Mol Recognit 2000, 13:223-278. 10.1002/1099-1352(200009/10)13:5<223::AID-JMR501>3.0.CO;2-L, 10992290.
32. Ascoli M, Fanelli F, Segaloff DL. The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr Rev 2002, 23:141-174. 10.1210/er.23.2.141, 11943741.
33. Kumar P, Sait SF, Sharma A, Kumar M. Ovarian hyperstimulation syndrome. J Hum Reprod Sci 2011, 4:70-75. 10.4103/0974-1208.86080, 3205536, 22065820.
34. Cerrillo M, Pacheco A, Rodriguez S, Gomez R, Delgado F, Pellicer A, Garcia-Velasco JA. Effect of GnRH agonist and hCG treatment on VEGF, angiopoietin-2, and VE-cadherin: trying to explain the link to ovarian hyperstimulation syndrome. Fertil Steril 2011, 95:2517-2519. 10.1016/j.fertnstert.2010.12.054, 21269615.
35. Vardhana PA, Julius MA, Pollak SV, Lustbader EG, Trousdale RK, Lustbader JW. A unique human chorionic gonadotropin antagonist suppresses ovarian hyperstimulation syndrome in rats. Endocrinology 2009, 150:3807-3814. 10.1210/en.2009-0107, 2717881, 19443574.
36. Van de Lagemaat R, Raafs BC, Van Koppen C, Timmers CM, Mulders SM, Hanssen RG. Prevention of the onset of ovarian hyperstimulation syndrome (OHSS) in the rat after ovulation induction with a low molecular weight agonist of the LH receptor compared with hCG and rec-LH. Endocrinology 2011, 152:4350-4357. 10.1210/en.2011-1077, 21896671.
37. Fanelli F, Puett D. Structural aspects of luteinizing hormone receptor: information from molecular modeling and mutagenesis. Endocrine 2002, 18:285-293. 10.1385/ENDO:18:3:285, 12450321.
38. Fanelli F, Themmen AP, Puett D. Lutropin receptor function: insights from natural, engineered, and computer-simulated mutations. IUBMB Life 2001, 51:149-155. 10.1080/152165401753544214, 11547916.
39. Fanelli F, Verhoef-Post M, Timmerman M, Zeilemaker A, Martens JW, Themmen AP. Insight into mutation-induced activation of the luteinizing hormone receptor: molecular simulations predict the functional behavior of engineered mutants at M398. Mol Endocrinol 2004, 18:1499-1508. 10.1210/me.2003-0050, 15016840.
40. Themmen AP. An update of the pathophysiology of human gonadotrophin subunit and receptor gene mutations and polymorphisms. Reprod Suppl 2005, 130:263-274.
41. Minegishi T, Nakamura K, Takakura Y, Miyamoto K, Hasegawa Y, Ibuki Y, Igarashi M, Minegish T. Cloning and sequencing of human LH/hCG receptor cDNA. Biochem Biophys Res Commun 1990, 172:1049-1054. 10.1016/0006-291X(90)91552-4, 2244890.
42. Atger M, Misrahi M, Sar S, Le Flem L, Dessen P, Milgrom E. Structure of the human luteinizing hormone-choriogonadotropin receptor gene: unusual promoter and 5' non-coding regions. Mol Cell Endocrinol 1995, 111:113-123. 10.1016/0303-7207(95)03557-N, 7556872.
43. Mongan NP, Hughes IA, Lim HN. Evidence that luteinising hormone receptor polymorphisms may contribute to male undermasculinisation. Eur J Endocrinol 2002, 147:103-107. 10.1530/eje.0.1470103, 12088926.
44. Bentov Y, Kenigsberg S, Casper RF. A novel luteinizing hormone/chorionic gonadotropin receptor mutation associated with amenorrhea, low oocyte yield, and recurrent pregnancy loss. Fertil Steril 2012, 97:1165-1168. 10.1016/j.fertnstert.2012.02.002, 22369774.
45. Simoni M, Tuttelmann F, Michel C, Bockenfeld Y, Nieschlag E, Gromoll J. Polymorphisms of the luteinizing hormone/chorionic gonadotropin receptor gene: association with maldescended testes and male infertility. Pharmacogenet Genomics 2008, 18:193-200. 10.1097/FPC.0b013e3282f4e98c, 18300940.
46. Kossack N, Troppmann B, Richter-Unruh A, Kleinau G, Gromoll J. Aberrant transcription of the LHCGR gene caused by a mutation in exon 6A leads to Leydig cell hypoplasia type II. Mol Cell Endocrinol 2013, 366:59-67. 10.1016/j.mce.2012.11.018, 23232123.
47. Latronico AC, Arnhold IJ. Inactivating mutations of the human luteinizing hormone receptor in both sexes. Semin Reprod Med 2012, 30:382-386. 10.1055/s-0032-1324721, 23044874.
48. Yariz KO, Walsh T, Uzak A, Spiliopoulos M, Duman D, Onalan G, King MC, Tekin M. Inherited mutation of the luteinizing hormone/choriogonadotropin receptor (LHCGR) in empty follicle syndrome. Fertil Steril 2011, 96:e125-130. 10.1016/j.fertnstert.2011.05.057, 3143235, 21683950.
49. Qiao J, Han B, Liu BL, Chen X, Ru Y, Cheng KX, Chen FG, Zhao SX, Liang J, Lu YL, et al. A splice site mutation combined with a novel missense mutation of LHCGR cause male pseudohermaphroditism. Hum Mutat 2009, 30:E855-865. 10.1002/humu.21072, 19551906.
50. Arnhold IJ, Lofrano-Porto A, Latronico AC. Inactivating mutations of luteinizing hormone beta-subunit or luteinizing hormone receptor cause oligo-amenorrhea and infertility in women. Horm Res 2009, 71:75-82.
51. Segaloff DL. Diseases associated with mutations of the human lutropin receptor. Prog Mol Biol Transl Sci 2009, 89:97-114.
52. Piersma D, Berns EM, Verhoef-Post M, Uitterlinden AG, Braakman I, Pols HA, Themmen AP. A common polymorphism renders the luteinizing hormone receptor protein more active by improving signal peptide function and predicts adverse outcome in breast cancer patients. J Clin Endocrinol Metab 2006, 91:1470-1476. 10.1210/jc.2005-2156, 16464948.
53. Piersma D, Themmen AP, Look MP, Klijn JG, Foekens JA, Uitterlinden AG, Pols HA, Berns EM. GnRH and LHR gene variants predict adverse outcome in premenopausal breast cancer patients. Breast Cancer Res 2007, 9:R51. 10.1186/bcr1756, 2206727, 17692113.
54. Rodien P, Cetani F, Costagliola S, Tonacchera M, Duprez L, Minegishi T, Govaerts C, Vassart G. Evidences for an allelic variant of the human LC/CG receptor rather than a gene duplication: functional comparison of wild-type and variant receptors. J Clin Endocrinol Metab 1998, 83:4431-4434. 10.1210/jc.83.12.4431, 9851790.
55. Tsai-Morris CH, Geng Y, Buczko E, Dehejia A, Dufau ML. Genomic distribution and gonadal mRNA expression of two human luteinizing hormone receptor exon 1 sequences in random populations. Hum Hered 1999, 49:48-51. 10.1159/000022840, 9858858.
56. Chen ZJ, Zhao H, He L, Shi Y, Qin Y, Shi Y, Li Z, You L, Zhao J, Liu J, et al. Genome-wide association study identifies susceptibility loci for polycystic ovary syndrome on chromosome 2p16.3, 2p21 and 9q33.3. Nat Genet 2011, 43:55-59. 10.1038/ng.732, 21151128.
57. Kerkela E, Skottman H, Friden B, Bjuresten K, Kere J, Hovatta O. Exclusion of coding-region mutations in luteinizing hormone and follicle-stimulating hormone receptor genes as the cause of ovarian hyperstimulation syndrome. Fertil Steril 2007, 87:603-606. 10.1016/j.fertnstert.2006.06.060, 17074323.
58. Bergh PA, Navot D. Ovarian hyperstimulation syndrome: a review of pathophysiology. J Assist Reprod Genet 1992, 9:429-438. 10.1007/BF01204048, 1482837.
59. Navot D, Bergh PA, Laufer N. Ovarian hyperstimulation syndrome in novel reproductive technologies: prevention and treatment. Fertil Steril 1992, 58:249-261.
60. Westfall PH, Wolfinger RD Closed multiple testing procedures and PROC MULTTEST 2000, Estados Unidos: Observations SAS Institute Inc., Westfall PH, Wolfinger RD.
61. Lancaster AK, Single RM, Solberg OD, Nelson MP, Thomson G. PyPop update-a software pipeline for large-scale multilocus population genomics. Tissue Antigens 2007, 69(Suppl 1):192-197.
62. Gaunt TR, Rodriguez S, Day IN. Cubic exact solutions for the estimation of pairwise haplotype frequencies: implications for linkage disequilibrium analyses and a web tool 'CubeX'. BMC Bioinformatics 2007, 8:428. 10.1186/1471-2105-8-428, 2180187, 17980034.
63. Achrekar SK, Modi DN, Desai SK, Mangoli VS, Mangoli RV, Mahale SD. Follicle-stimulating hormone receptor polymorphism (Thr307Ala) is associated with variable ovarian response and ovarian hyperstimulation syndrome in Indian women. Fertil Steril 2009, 91:432-439. 10.1016/j.fertnstert.2007.11.093, 18321487.
64. d'Alva CB, Serafini P, Motta E, Kohek MB, Latronico AC, Mendonca BB. Absence of follicle-stimulating hormone receptor activating mutations in women with iatrogenic ovarian hyperstimulation syndrome. Fertil Steril 2005, 83:1695-1699. 10.1016/j.fertnstert.2004.12.044, 15950638.
65. Moron FJ, De Castro F, Royo JL, Montoro L, Mira E, Saez ME, Real LM, Gonzalez A, Manes S, Ruiz A. Bone morphogenetic protein 15 (BMP15) alleles predict over-response to recombinant follicle stimulation hormone and iatrogenic ovarian hyperstimulation syndrome (OHSS). Pharmacogenet Genomics 2006, 16:485-495. 10.1097/01.fpc.0000215073.44589.96, 16788381.
66. Hanevik HI, Hilmarsen HT, Skjelbred CF, Tanbo T, Kahn JA. Increased risk of ovarian hyperstimulation syndrome following controlled ovarian hyperstimulation in patients with vascular endothelial growth factor +405 cc genotype. Gynecol Endocrinol 2012, 28:845-849. 10.3109/09513590.2012.683056, 22587628.
67. Haasl RJ, Ahmadi MR, Meethal SV, Gleason CE, Johnson SC, Asthana S, Bowen RL, Atwood CS. A luteinizing hormone receptor intronic variant is significantly associated with decreased risk of Alzheimer's disease in males carrying an apolipoprotein E epsilon4 allele. BMC Med Genet 2008, 9:37. 2396156, 18439297.
68. Corbo RM, Ulizzi L, Scacchi R, Martinez-Labarga C, De Stefano GF. Apolipoprotein E polymorphism and fertility: a study in pre-industrial populations. Mol Hum Reprod 2004, 10:617-620. 10.1093/molehr/gah082, 15220465.
69. Corbo RM, Ulizzi L, Piombo L, Scacchi R. Study on a possible effect of four longevity candidate genes (ACE, PON1, PPAR-gamma, and APOE) on human fertility. Biogerontology 2008, 9:317-323. 10.1007/s10522-008-9143-9, 18443916.
70. Corbo RM, Scacchi R, Cresta M. Differential reproductive efficiency associated with common apolipoprotein e alleles in postreproductive-aged subjects. Fertil Steril 2004, 81:104-107. 10.1016/j.fertnstert.2003.05.029, 14711551.