Male Reproductive Cancers pp 317-335 | Cite as
Susceptibility Alleles for Testicular Germ Cell Tumor
Abstract
A family history of Testicular Germ Cell Tumor (TGCT) is among the strongest and most well-documented risk factors for TGCT (Forman et al. 1992; Westergaard et al. 1996; Heimdal et al. 1996; Sonneveld et al. 1999; Hemminki and Li 2004). In a proportion of cases (∼2%), a first-degree family member is also affected with the disease (Forman et al. 1992). The relative risk to a brother of a TGCT case is 8–10 and between fathers and sons is 4–6 (Forman et al. 1992; Heimdal et al. 1996; Hemminki and Li 2004). This relative risk is higher than for most other cancer types, which are commonly 2 and rarely exceed 4 (Dong and Hemminki 2001). The high relative risk suggests that susceptibility genes are involved in the etiology of TGCT, which cannot be accounted for solely by shared environmental factors.
Keywords
Testicular Germ Cell Tumor High Relative Risk Androgen Insensitivity Syndrome Testicular Microlithiasis Shared Environmental FactorReferences
- Asada Y, Varnum DS, Frankel WN, Nadeau JH (1994) A mutation in the Ter gene causing increased susceptibility to testicular teratomas maps to mouse chromosome 18. Nat Genet 6:363–368PubMedCrossRefGoogle Scholar
- Bianchi NO, Richard SM, Pavicic W (2006) Y chromosome instability in testicular cancer. Mutat Res 612:172–188PubMedCrossRefGoogle Scholar
- Bianchi NO, Richard SM, Peltomaki P, Bianchi MS (2002) Mosaic AZF deletions and susceptibility to testicular tumors. Mutat Res 503:51–62PubMedCrossRefGoogle Scholar
- Bosl GJ, Motzer RJ (1997) Testicular germ-cell cancer. N Engl J Med 337:242–253PubMedCrossRefGoogle Scholar
- Carvalho CM, Zuccherato LW, Bastos-Rodrigues L, Santos FR, Pena SD (2006) No association found between gr/gr deletions and infertility in Brazilian males. Mol Hum Reprod 12:269–273PubMedCrossRefGoogle Scholar
- Chen CP, Chern SR, Wang TY, Wang W, Wang KL, Jeng CJ (1999) Androgen receptor gene mutations in 46, XY females with germ cell tumours. Hum Reprod 14:664–670PubMedCrossRefGoogle Scholar
- Coffey J, Huddart R, Elliott F, Sohaib AS, Parker E, Dudakia D, Pugh J, Easton DF, Bishop DT, Stratton MR, Rapley EA (2007) Testicular microlithiasis as a familial risk factor for testicular germ cell tumour. BJC. Br J Cancer. 97:1701–6Google Scholar
- Coffey J, Huddart RA, Norman AR, Dudakia D, Stratton M, Rapley EA (2006) Characteristics of a single-centre series of familial testicular germ cell tumours. ASCO Annual Meeting Proceedings. J Clin Oncol 24 (Abst. no. 10039)Google Scholar
- Crockford GP, Linger R, Hockley S, Dudakia D, Johnson L, Huddart R, Tucker K, Friedlander M, Phillips KA, Hogg D, Jewett MA, Lohynska R, Daugaard G, Richard S, Chompret A, Bonaiti-Pellie C, Heidenreich A, Albers P, Olah E, Geczi L, Bodrogi I, Ormiston WJ, Daly PA, Guilford P, Fossa SD, Heimdal K, Tjulandin SA, Liubchenko L, Stoll H, Weber W, Forman D, Oliver T, Einhorn L, McMaster M, Kramer J, Greene MH, Weber BL, Nathanson KL, Cortessis V, Easton DF, Bishop DT, Stratton MR, Rapley EA (2006) Genome-wide linkage screen for testicular germ cell tumour susceptibility loci. Hum Mol Genet 15:443–451PubMedCrossRefGoogle Scholar
- de Carvalho CM, Zuccherato LW, Fujisawa M, Shirakawa T, Ribeiro-dos-Santos AK, Santos SE, Pena SD, Santos FR (2006) Study of AZFc partial deletion gr/gr in fertile and infertile Japanese males. J Hum Genet 51:794–799PubMedCrossRefGoogle Scholar
- de Llanos M, Ballesca JL, Gazquez C, Margarit E, Oliva R (2005) High frequency of gr/gr chromosome Y deletions in consecutive oligospermic ICSI candidates. Hum Reprod 20:216–220PubMedCrossRefGoogle Scholar
- Dong C, Hemminki K (2001) Modification of cancer risks in offspring by sibling and parental cancers from 2, 112, 616 nuclear families. Int J Cancer 92:144–150PubMedCrossRefGoogle Scholar
- Easton DF, Pooley KA, Dunning AM, Pharoah PD, Thompson D, Ballinger DG, Struewing JP, Morrison J, Field H, Luben R, Wareham N, Ahmed S, Healey CS, Bowman R, Luccarini C, Conroy D, Shah M, Munday H, Jordan C, Perkins B, West J, Redman K, Meyer KB, Haiman CA, Kolonel LK, Henderson BE, Le Marchand L, Brennan P, Sangrajrang S, Gaborieau V, Odefrey F, Shen CY, Wu PE, Wang HC, Eccles D, Evans DG, Peto J, Fletcher O, Johnson N, Seal S, Stratton MR, Rahman N, Chenevix-Trench G, Bojesen SE, Nordestgaard BG, Axelsson CK, Garcia-Closas M, Brinton L, Chanock S, Lissowska J, Peplonska B, Nevanlinna H, Fagerholm R, Eerola H, Kang D, Yoo KY, Noh DY, Ahn SH, Hunter DJ, Hankinson SE, Cox DG, Hall P, Wedren S, Liu J, Low YL, Bogdanova N, Schurmann P, Dork T, Tollenaar RA, Jacobi CE, Devilee P, Klijn JG, Sigurdson AJ, Doody MM, Alexander BH, Zhang J, Cox A, Brock IW, Macpherson G, Reed MW, Couch FJ, Goode EL, Olson JE, Meijers-Heijboer H, van den OA, Uitterlinden A, Rivadeneira F, Milne RL, Ribas G, Gonzalez-Neira A, Benitez J, Hopper JL, McCredie M, Southey M, Giles GG, Schroen C, Justenhoven C, Brauch H, Hamann U, Ko YD, Spurdle AB, Beesley J, Chen X, Aghmesheh M, Amor D, Andrews L, Antill Y, Armes J, Armitage S, Arnold L, Balleine R, Begley G, Beilby J, Bennett I, Bennett B, Berry G, Blackburn A, Brennan M, Brown M, Buckley M, Burke J, Butow P, Byron K, Callen D, Campbell I, Chenevix-Trench G, Clarke C, Colley A, Cotton D, Cui J, Culling B, Cummings M, Dawson SJ, Dixon J, Dobrovic A, Dudding T, Edkins T, Eisenbruch M, Farshid G, Fawcett S, Field M, Firgaira F, Fleming J, Forbes J, Friedlander M, Gaff C, Gardner M, Gattas M, George P, Giles G, Gill G, Goldblatt J, Greening S, Grist S, Haan E, Harris M, Hart S, Hayward N, Hopper J, Humphrey E, Jenkins M, Jones A, Kefford R, Kirk J, Kollias J, Kovalenko S, Lakhani S, Leary J, Lim J, Lindeman G, Lipton L, Lobb L, Maclurcan M, Mann G, Marsh D, McCredie M, McKay M, Anne MS, Meiser B, Milne R, Mitchell G, Newman B, O’loughlin I, Osborne R, Peters L, Phillips K, Price M, Reeve J, Reeve T, Richards R, Rinehart G, Robinson B, Rudzki B, Salisbury E, Sambrook J, Saunders C, Scott C, Scott E, Scott R, Seshadri R, Shelling A, Southey M, Spurdle A, Suthers G, Taylor D, Tennant C, Thorne H, Townshend S, Tucker K, Tyler J, Venter D, Visvader J, Walpole I, Ward R, Waring P, Warner B, Warren G, Watson E, Williams R, Wilson J, Winship I, Young MA, Bowtell D, Green A, Defazio A, Chenevix-Trench G, Gertig D, Webb P, Mannermaa A, Kosma VM, Kataja V, Hartikainen J, Day NE, Cox DR, Ponder BA (2007) Genome-wide association study identifies novel breast cancer susceptibility loci. Nature 447(7148):1087–1093PubMedCrossRefGoogle Scholar
- Ferlin A, Tessari A, Ganz F, Marchina E, Barlati S, Garolla A, Engl B, Foresta C (2005) Association of partial AZFc region deletions with spermatogenic impairment and male infertility. J Med Genet 42:209–213PubMedCrossRefGoogle Scholar
- Forman D, Gallagher R, Moller H, Swerdlow TJ (1990) Aetiology and epidemiology of testicular cancer: report of consensus group. Prog Clin Biol Res 357:245–253PubMedGoogle Scholar
- Forman D, Oliver RT, Brett AR, Marsh SG, Moses JH, Bodmer JG, Chilvers CE, Pike MC (1992) Familial testicular cancer: a report of the UK family register, estimation of risk and an HLA class 1 sib-pair analysis. Br J Cancer 65:255–262PubMedCrossRefGoogle Scholar
- Frydelund-Larsen L, Vogt PH, Leffers H, Schadwinkel A, Daugaard G, Skakkebaek NE, Rajpert-De Meyts E (2003) No AZF deletion in 160 patients with testicular germ cell neoplasia. Mol Hum Reprod 9:517–521PubMedCrossRefGoogle Scholar
- Gajendran VK, Nguyen M, Ellison LM (2005) Testicular cancer patterns in African-American men. Urology 66:602–605PubMedCrossRefGoogle Scholar
- Garolla A, Ferlin A, Vinanzi C, Roverato A, Sotti G, Artibani W, Foresta C (2005) Molecular analysis of the androgen receptor gene in testicular cancer. Endocr Relat Cancer 12:645–655PubMedCrossRefGoogle Scholar
- Gedde-Dahl TJ, Hannisdal E, Klepp OH, Grottum KA, Waksvik H, Fossa SD, Stenwig AE, Broogger A (1985) Testicular neoplasms occurring in four brothers. A search for a genetic predisposition. Cancer 55:2005–2009PubMedCrossRefGoogle Scholar
- Giwercman A, Lundin KB, Eberhard J, Stahl O, Cwikiel M, Cavallin-Stahl E, Giwercman YL (2004) Linkage between androgen receptor gene CAG trinucleotide repeat length and testicular germ cell cancer histological type and clinical stage. Eur J Cancer 40:2152–2158PubMedCrossRefGoogle Scholar
- Goss PE, Bulbul MA (1990) Familial testicular cancer in five members of a cancer-prone kindred. Cancer 66:2044–2046PubMedCrossRefGoogle Scholar
- Harland SJ, Daugaard G, Horwich A, Mead GM, Fossa S, Sokal M, Morgenstern D, Oliver R, Cook P, Stenning SP (2006) The familial influence on bilateral testicular germ cell cancer: medical research council study TER2. Annual Meeting Proceedings. J Clin Oncol 24:239s (Abst. no. 4590)Google Scholar
- Heimdal K, Fossa SD (1994) Genetic factors in malignant germ-cell tumors. World J Urol 12:178–181PubMedCrossRefGoogle Scholar
- Heimdal K, Olsson H, Tretli S, Flodgren P, Borresen AL, Fossa SD (1996) Familial testicular cancer in Norway and southern Sweden. Br J Cancer 73:964–969PubMedCrossRefGoogle Scholar
- Heimdal K, Olsson H, Tretli S, Fossa SD, Borresen AL, Bishop DT (1997) A segregation analysis of testicular cancer based on Norwegian and Swedish families. Br J Cancer 75:1084–1087PubMedCrossRefGoogle Scholar
- Heimdal KR, Lothe RA, Fossa SD, Borresen AL (1994) Association studies of a polymorphism in the Wilms’ tumor 1 locus in Norwegian patients with testicular cancer. Int J Cancer 58:523–526PubMedCrossRefGoogle Scholar
- Hemminki K, Li X (2004) Familial risk in testicular cancer as a clue to a heritable and environmental aetiology. Br J Cancer 90:1765–1770PubMedCrossRefGoogle Scholar
- Hirschhorn JN, Daly MJ (2005) Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6:95–108PubMedCrossRefGoogle Scholar
- Holzik MF, Rapley EA, Hoekstra HJ, Sleijfer DT, Nolte IM, Sijmons RH (2004) Genetic predisposition to testicular germ-cell tumours. Lancet Oncol 5:363–371CrossRefGoogle Scholar
- Houlston RS, Peto J (2003) The future of association studies of common cancers. Hum Genet 112:434–435PubMedGoogle Scholar
- Hucklenbroich K, Gromoll J, Heinrich M, Hohoff C, Nieschlag E, Simoni M (2005) Partial deletions in the AZFc region of the Y chromosome occur in men with impaired as well as normal spermatogenesis. Hum Reprod 20:191–197PubMedCrossRefGoogle Scholar
- Jacobsen R, Bostofte E, Engholm G, Hansen J, Olsen JH, Skakkebaek NE, Moller H (2000) Risk of testicular cancer in men with abnormal semen characteristics: cohort study. BMJ 321:789–792PubMedCrossRefGoogle Scholar
- Kanetsky PA, Mitra N, Vardhanabhuti S, Li M, Vaughn DJ, Letrero R, Ciosek SL, Doody DR, Smith LM, Weaver J, Albano A, Chen C, Starr JR, Rader DJ, Godwin AK, Reilly MP, Hakonarson H, Schwartz SM, Nathanson KL. (2009) Common variation in KITLG and at 5q31.3 predisposes to testicular germ cell cancer. Nat Genet. 41:811–5.Google Scholar
- Khoury MJ, Beaty TH, Liang KY (1988) Can familial aggregation of disease be explained by familial aggregation of environmental risk factors? Am J Epidemiol 127:674–683PubMedGoogle Scholar
- Kuroda-Kawaguchi T, Skaletsky H, Brown LG, Minx PJ, Cordum HS, Waterston RH, Wilson RK, Silber S, Oates R, Rozen S, Page DC (2001) The AZFc region of the Y chromosome features massive palindromes and uniform recurrent deletions in infertile men. Nat Genet 29:279–286PubMedCrossRefGoogle Scholar
- Levin HS (2000) Tumors of the testis in intersex syndromes. Urol Clin North Am 27:543–551, xGoogle Scholar
- Lichtenstein P, Holm NV, Verkasalo PK, Iliadou A, Kaprio J, Koskenvuo M, Pukkala E, Skytthe A, Hemminki K (2000) Environmental and heritable factors in the causation of cancer – analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med 343:78–85PubMedCrossRefGoogle Scholar
- Linger R, Dudakia D, Huddart R, Tucker K, Friedlander M, Phillips K-A, Hogg D, Jewett MAS, Lohynska R, Daugaard G, Richard S, Chompret A, Stoppa-Lyonnet D, Bonaiti-Pellie C, Heidenreich A, Albers P, Olah E, Geczi L, Bodrogi I, Daly PA, Guildford P, Fossa S, Heimdal K, Tjulandin SA, Liubchenko L, Stoll H, Weber W, Einhorn L, McMaster M, Korde L, Greene MH, Nathanson KL, Cortessis V, Easton DF, Bishop DT, Stratton MR, Rapley EA (2007a) Analysis of the DND1 gene in men with sporadic and familial testicular germ cell tumours. Genes Chromosomes Cancer. 2008 47:247–52.Google Scholar
- Linger R, Dudakia D, Huddart R, Easton D, Bishop DT, Stratton MR, Rapley EA (2007b) A physical analysis of the Y chromosome shows no additional deletions, other than Gr/Gr, associated with testicular germ cell tumour. Br J Cancer 96:357–361PubMedCrossRefGoogle Scholar
- Lutke Holzik MF, Storm K, Sijmons RH, D’hollander M, Arts EG, Verstraaten ML, Sleijfer DT, Hoekstra HJ (2005) Absence of constitutional Y chromosome AZF deletions in patients with testicular germ cell tumors. Urology 65:196–201PubMedCrossRefGoogle Scholar
- Lynch M, Cram DS, Reilly A, O’Bryan MK, Baker HW, de Kretser DM, McLachlan RI (2005) The Y chromosome gr/gr subdeletion is associated with male infertility. Mol Hum Reprod 11:507–512PubMedCrossRefGoogle Scholar
- Machev N, Saut N, Longepied G, Terriou P, Navarro A, Levy N, Guichaoua M, Metzler-Guillemain C, Collignon P, Frances AM, Belougne J, Clemente E, Chiaroni J, Chevillard C, Durand C, Ducourneau A, Pech N, McElreavey K, Mattei MG, Mitchell MJ (2004) Sequence family variant loss from the AZFc interval of the human Y chromosome, but not gene copy loss, is strongly associated with male infertility. J Med Genet 41:814–825PubMedCrossRefGoogle Scholar
- Matin A, Nadeau JH (2005) Search for testicular cancer gene hits dead-end. Cell Cycle 4:1136–1138PubMedCrossRefGoogle Scholar
- McGlynn KA, Devesa SS, Graubard BI, Castle PE (2005) Increasing incidence of testicular germ cell tumors among black men in the United States. J Clin Oncol 23:5757–5761PubMedCrossRefGoogle Scholar
- Nathanson KL, Kanetsky PA, Hawes R, Vaughn DJ, Letrero R, Tucker K, Friedlander M, Phillips KA, Hogg D, Jewett MA, Lohynska R, Daugaard G, Richard S, Chompret A, Bonaiti-Pellie C, Heidenreich A, Olah E, Geczi L, Bodrogi I, Ormiston WJ, Daly PA, Oosterhuis JW, Gillis AJ, Looijenga LH, Guilford P, Fossa SD, Heimdal K, Tjulandin SA, Liubchenko L, Stoll H, Weber W, Rudd M, Huddart R, Crockford GP, Forman D, Oliver DT, Einhorn L, Weber BL, Kramer J, McMaster M, Greene MH, Pike M, Cortessis V, Chen C, Schwartz SM, Bishop DT, Easton DF, Stratton MR, Rapley EA (2005) The Y deletion gr/gr and susceptibility to testicular germ cell tumor. Am J Hum Genet 77:1034–1043PubMedCrossRefGoogle Scholar
- Nicholson PW, Harland SJ (1995) Inheritance and testicular cancer. Br J Cancer 71:421–426PubMedCrossRefGoogle Scholar
- Petersen PM, Skakkebaek NE, Giwercman A (1998) Gonadal function in men with testicular cancer: biological and clinical aspects. APMIS 106:24–34PubMedCrossRefGoogle Scholar
- Purdue MP, Sakoda LC, Graubard BI, Welch R, Chanock SJ, Sesterhenn IA, Rubertone MV, Erickson RL, McGlynn KA (2007) A case-control investigation of immune function gene polymorphisms and risk of testicular germ cell tumors. Cancer Epidemiol Biomarkers Prev 16:77–83PubMedCrossRefGoogle Scholar
- Rajpert-De Meyts E, Leffers H, Daugaard G, Andersen CB, Petersen PM, Hinrichsen J, Pedersen LG, Skakkebaek NE (2002) Analysis of the polymorphic CAG repeat length in the androgen receptor gene in patients with testicular germ cell cancer. Int J Cancer 102:201–204PubMedCrossRefGoogle Scholar
- Rapley EA, Crockford GP, Teare D, Biggs P, Seal S, Barfoot R, Edwards S, Hamoudi R, Heimdal K, Fossa SD, Tucker K, Donald J, Collins F, Friedlander M, Hogg D, Goss P, Heidenreich A, Ormiston W, Daly PA, Forman D, Oliver TD, Leahy M, Huddart R, Cooper CS, Bodmer JG (2000) Localization to Xq27 of a susceptibility gene for testicular germ-cell tumours. Nat Genet 24(2):197–200PubMedCrossRefGoogle Scholar
- Rapley EA, Turnbull C, Al Olama AA, Dermitzakis ET, Linger R, Huddart RA, Renwick A, Hughes D, Hines S, Seal S, Morrison J, Nsengimana J, Deloukas P; UK Testicular Cancer Collaboration, Rahman N, Bishop DT, Easton DF, Stratton MR. (2009) A genome-wide association study of testicular germ cell tumor. Nat Genet. 41:807–10.Google Scholar
- Repping S, Skaletsky H, Brown L, van Daalen SK, Korver CM, Pyntikova T, Kuroda-Kawaguchi T, de Vries JW, Oates RD, Silber S, van der Veen F, Page DC, Rozen S (2003) Polymorphism for a 1.6-Mb deletion of the human Y chromosome persists through balance between recurrent mutation and haploid selection. Nat Genet 35:247–251PubMedCrossRefGoogle Scholar
- Richard SM, Bianchi NO, Bianchi MS, Peltomaki P, Lothe RA, Pavicic W (2004) Ethnic variation in the prevalence of AZF deletions in testicular cancer. Mutat Res 554:45–51PubMedCrossRefGoogle Scholar
- Richiardi L, Akre O (2005) Fertility among brothers of patients with testicular cancer. Cancer Epidemiol Biomarkers Prev 14:2557–2562PubMedCrossRefGoogle Scholar
- Richiardi L, Pettersson A, Akre O (2007) Genetic and environmental risk factors for testicular cancer. Int J Androl 30(4):230–240PubMedCrossRefGoogle Scholar
- Sakai N, Yamada T, Asao T, Baba M, Yoshida M, Murayama T (2000) Bilateral testicular tumors in androgen insensitivity syndrome. Int J Urol 7:390–392PubMedCrossRefGoogle Scholar
- Sakurai T, Iguchi T, Moriwaki K, Noguchi M (1995) The ter mutation first causes primordial germ cell deficiency in ter/ter mouse embryos at 8 days of gestation. Dev Growth Differ 37:293–302CrossRefGoogle Scholar
- Senturia YD (1987) The epidemiology of testicular cancer. Br J Urol 60:285–291PubMedCrossRefGoogle Scholar
- Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T, Chinwalla A, Delehaunty A, Delehaunty K, Du H, Fewell G, Fulton L, Fulton R, Graves T, Hou SF, Latrielle P, Leonard S, Mardis E, Maupin R, McPherson J, Miner T, Nash W, Nguyen C, Ozersky P, Pepin K, Rock S, Rohlfing T, Scott K, Schultz B, Strong C, Tin-Wollam A, Yang SP, Waterston RH, Wilson RK, Rozen S, Page DC (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423:825–837PubMedCrossRefGoogle Scholar
- Sonneveld DJ, Sleijfer DT, Schrafford KH, Sijmons RH, van der Graaf WT, Sluiter WJ, Hoekstra HJ (1999) Familial testicular cancer in a single-centre population. Eur J Cancer 35:1368–1373PubMedCrossRefGoogle Scholar
- Starr JR, Chen C, Doody DR, Hsu L, Ricks S, Weiss NS, Schwartz SM (2005) Risk of testicular germ cell cancer in relation to variation in maternal and offspring cytochrome p450 genes involved in catechol estrogen metabolism. Cancer Epidemiol Biomarkers Prev 14:2183–2190PubMedCrossRefGoogle Scholar
- Stevens LC (1973) A new inbred subline of mice (129-terSv) with a high incidence of spontaneous congenital testicular teratomas. J Natl Cancer Inst 50:235–242PubMedGoogle Scholar
- Swerdlow AJ, De Stavola BL, Swanwick MA, Maconochie NE (1997) Risks of breast and testicular cancers in young adult twins in England and Wales: evidence on prenatal and genetic aetiology. Lancet 350:1723–1728PubMedCrossRefGoogle Scholar
- Tollerud DJ, Blattner WA, Fraser MC, Brown LM, Pottern L, Shapiro E, Kirkemo A, Shawker TH, Javadpour N, O’Connell K (1985) Familial testicular cancer and urogenital developmental anomalies. Cancer 55:1849–1854PubMedCrossRefGoogle Scholar
- The International HapMap Project (2003) Nature 426:789–796Google Scholar
- The Wellcome Trust Case Control Consortium (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447:661–678CrossRefGoogle Scholar
- Vogt PH, Edelmann A, Kirsch S, Henegariu O, Hirschmann P, Kiesewetter F, Kohn FM, Schill WB, Farah S, Ramos C, Hartmann M, Hartschuh W, Meschede D, Behre HM, Castel A, Nieschlag E, Weidner W, Grone HJ, Jung A, Engel W, Haidl G (1996) Human Y chromosome azoospermia factors (AZF) mapped to different subregions in Yq11. Hum Mol Genet 5:933–943PubMedCrossRefGoogle Scholar
- Westergaard T, Olsen JH, Frisch M, Kroman N, Nielsen JW, Melbye M (1996) Cancer risk in fathers and brothers of testicular cancer patients in Denmark. A population-based study. Int J Cancer 66:627–631PubMedCrossRefGoogle Scholar
- Youngren KK, Coveney D, Peng X, Bhattacharya C, Schmidt LS, Nickerson ML, Lamb BT, Deng JM, Behringer RR, Capel B, Rubin EM, Nadeau JH, Matin A (2005) The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 435:360–364PubMedCrossRefGoogle Scholar
- Zhang F, Li Z, Wen B, Jiang J, Shao M, Zhao Y, He Y, Song X, Qian J, Lu D, Jin L (2006) A frequent partial AZFc deletion does not render an increased risk of spermatogenic impairment in East Asians. Ann Hum Genet 70:304–313PubMedCrossRefGoogle Scholar