The role of microenvironment in testicular germ cell tumors

Cancer Biology and Therapy

Volumn 10, Issue 6, 2010, Pages 529-536

  Díez Torre, Alejandro ^a   Silván, Unai ^a   Díaz Núñez, María ^a   Aréchaga, Juan ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Hypoxia; Testicular germ cell tumor; Tumor invasion; Tumor microenvironment

Indexed keywords

ANTINEOPLASTIC AGENT; FIBROBLAST GROWTH FACTOR 9; GELATINASE A; GELATINASE B; SOMATOMEDIN; SOMATOMEDIN B; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN C; VASCULOTROPIN;

ANGIOGENESIS; CANCER GROWTH; CANCER INCIDENCE; CANCER RADIOTHERAPY; CARCINOMA IN SITU; CELL DIFFERENTIATION; CELL HYPOXIA; CELL PROLIFERATION; EXTRACELLULAR MATRIX; GERM CELL TUMOR; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NONHUMAN; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; RISK FACTOR; SEMINOMA; STROMA CELL; TESTIS; TESTIS CANCER; TESTIS CARCINOMA IN SITU; TESTIS NONSEMINOMA CANCER; TUMOR CELL; TUMOR LOCALIZATION; TUMOR MICROENVIRONMENT;

CARCINOMA IN SITU; CHEMOKINE CXCL12; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MALE; NEOPLASMS, GERM CELL AND EMBRYONAL; SIGNAL TRANSDUCTION; TESTICULAR NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 77957135244     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.10.6.13227     Document Type: Review

References (86)

1. Wu X, Groves FD, McLaughlin CC, Jemal A, Martin J, Chen VW. Cancer incidence patterns among adolescents and young adults in the United States. Cancer Causes Control 2005; 16:309-20. (Pubitemid 40897850)
2. Chia VM, Quraishi SM, Devesa SS, Purdue MP, Cook MB, McGlynn KA. International trends in the incidence of testicular cancer 1973-2002. Cancer Epidemiol Biomarkers Prev 2010; 19:1151-9.
3. Townsend JS, Richardson LC, German RR. Incidence of Testicular Cancer in the United States 1999-2004. Am J Mens Health 2009; [Epub ahead of print].
4. Walschaerts M, Huyghe E, Muller A, Bachaud JM, Bujan L, Thonneau P. Doubling of testicular cancer incidence rate over the last 20 years in Southern France. Cancer Causes Control 2008; 19:155-61.
5. Greene MH, Kratz CP, Mai PL, Mueller C, Peters JA, Bratslavsky G, et al. Familial testicular germ cell tumors in adults: 2010 summary of genetic risk factors and clinical phenotype. Endocr Relat Cancer 2010; 17:109-21.
6. Richiardi L, Pettersson A, Akre O. Genetic and environmental risk factors for testicular cancer. Int J Androl 2007; 30:230-40. (Pubitemid 47254401)
7. Oosterhuis JW, Looijenga LH. Testicular germ-cell tumours in a broader perspective. Nat Rev Cancer 2005; 5:210-22.
8. Aréchaga J. On the boundary between development and neoplasia. An interview with Professor G. Barry Pierce. Int J Dev Biol 1993; 37:5-16.
9. Andrews PW, Matin MM, Bahrami AR, Damjanov I, Gokhale P, Draper JS. Embryonic stem (ES) cells and embryonal carcinoma (EC) cells: opposite sides of the same coin. Biochem Soc Trans 2005; 33:1526-30.
10. Evans MJ, Kaufman MH. Establishment in culture of pluripotential calls from mouse embryos. Nature 1981; 292:154-6.
11. Bao S, Tang F, Li X, Hayashi K, Gillich A, Lao K, et al. Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells. Nature 2009; 461:1292-5.
12. Honecker F, Stoop H, Mayer F, Bokemeyer C, Castrillon DH, Lau YF, et al. Germ cell lineage differentiation in non-seminomatous germ cell tumours. J Pathol 2006; 208:395-400.
13. Silván U, Arlucea J, Andrade R, Díez-Torre A, Silió M, Konerding MA, et al. Angiogenesis and vascular network of teratocarcinoma from embryonic stem cell transplant into seminiferous tubules. Br J Cancer 2009; 101:64-70.
14. Silván U, Díez-Torre A, Andrade R, Arluzea J, Silió M, Aréchaga J. Embryonic stem cell transplantation into seminiferous tubules. A model for the study of invasive germ cell tumors of the testis. Cell Transpl 2010; (In press).
15. Hoei-Hansen CE, Rajpert-De Meyts E, Daugaard G, Skakkebaek NE. Carcinoma in situ testis, the progenitor of testicular germ cell tumours: a clinical review. Ann Oncol 2005; 16:863-8. (Pubitemid 40903910)
16. Sonne SB, Perrett RM, Nielsen JE, Baxter MA, Kristensen DM, Leffers H, et al. Analysis of SOX2 expression in developing human testis and germ cell neoplasia. Int J Dev Biol 2010; 54:755-60.
17. Manivel JC, Jessurun J, Wick MR, Dehner LP. Placental alkaline phosphatase immunoreactivity in testicular germ-cell neoplasms. Am J Surg Pathol 1987; 11:21-9.
18. Jacobsen GK, Henriksen OB, von der Maase H. Carcinoma in situ of testicular tissue adjacent to malignant germ-cell tumors: a study of 105 cases. Cancer 1981; 47:2660-2.
19. el Naggar AK, Ro JY, McLemore D, Ayala AG, Batsakis JG. DNA ploidy in testicular germ cell neoplasms: histogenetic and clinical implications. Am J Surg Pathol 1992; 16:611-8.
20. Skotheim RI, Lind GE, Monni O, Nesland JM, Abeler VM, Fossa SD, et al. Differentiation of human embryonal carcinomas in vitro and in vivo reveals expression profiles relevant to normal development. Cancer Res 2005; 65:5588-98.
21. Santagata S, Ligon KL, Hornick JL. Embryonic stem cell transcription factor signatures in the diagnosis of primary and metastatic germ cell tumors. Am J Surg Pathol 2007; 31:836-45. (Pubitemid 47165136)
22. Korkola JE, Houldsworth J, Chadalavada RS, Olshen AB, Dobrynski D, Reuter VE, et al. Downregulation of stem cell genes, including those in a 200-kb gene cluster at 12p13.31, is associated with in vivo differentiation of human male germ cell tumors. Cancer Res 2006; 66:820-7.
23. Baker DE, Harrison NJ, Maltby E, Smith K, Moore HD, Shaw PJ, et al. Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat Biotechnol 2007; 25:207-15.
24. Krausz C, Looijenga LH. Genetic aspects of testicular germ cell tumors. Cell Cycle 2008; 7:3519-24.
25. Looijenga LH, Rosenberg C, van Gurp RJ, Geelen E, Echten-Arends J, de Jong B, et al. Comparative genomic hybridization of microdissected samples from different stages in the development of a seminoma and a non-seminoma. J Pathol 2000; 191:187-92.
26. Summersgill B, Osin P, Lu YJ, Huddart R, Shipley J. Chromosomal imbalances associated with carcinoma in situ and associated testicular germ cell tumours of adolescents and adults. Brit J Cancer 2001; 85:213-20. (Pubitemid 32700297)
27. Ottesen AM, Skakkebaek NE, Lundsteen C, Leffers H, Larsen J, Rajpert-De Meyts E. High-resolution comparative genomic hybridization detects extra chromosome arm 12p material in most cases of carcinoma in situ adjacent to overt germ cell tumors, but not before the invasive tumor development. Genes Chromosomes Cancer 2003; 38:117-25.
28. Skotheim RI, Autio R, Lind GE, Kraggerud SM, Andrews PW, Monni O, et al. Novel genomic aberrations in testicular germ cell tumors by array-CGH, and associated gene expression changes. Cell Oncol 2006; 28:315-26.
29. Tanaka K, Okamoto S, Ishikawa Y, Tamura H, Hara T. DDX1 is required for testicular tumorigenesis, partially through the transcriptional activation of 12p stem cell genes. Oncogene 2009; 28:2142-51.
30. Beumer TL, Roepers-Gajadien HL, Gademan IS, Kal HB, de Rooij DG. Involvement of the D-type cyclins in germ cell proliferation and differentiation in the mouse. Biol Reprod 2000; 63:1893-8.
31. Hori H, Yano S, Koufuji K, Takeda J, Shirouzu K. CD9 expression in gastric cancer and its significance. J Surg Res 2004; 117:208-15. (Pubitemid 38393645)
32. Kawashima M, Doh-Ura K, Mekada E, Fukui M, Iwaki T. CD9 expression in solid non-neuroepithelial tumors and infiltrative astrocytic tumors. J Histochem Cytochem 2002; 50:1195-203. (Pubitemid 34988448)
33. Biermann K, Heukamp LC, Steger K, Zhou H, Franke FE, Sonnack V, et al. Genome-wide expression profiling reveals new insights into pathogenesis and progression of testicular germ cell tumors. Cancer Genom Proteom 2007; 4:359-67.
34. Skotheim RI, Monni O, Mousses S, Fossa SD, Kallioniemi OP, Lothe RA, et al. New insights into testicular germ cell tumorigenesis from gene expression profiling. Cancer Res 2002; 62:2359-64. (Pubitemid 34411718)
35. Velasco A, Riquelme E, Schultz M, Wistuba II, Villarroel L, Pizarro J, et al. Mismatch repair gene expression and genetic instability in testicular germ cell tumor. Cancer Biol Ther 2004; 3:977-82.
36. Velasco A, Riquelme E, Schultz M, Wistuba II, Villarroel L, Koh MS, et al. Microsatellite instability and loss of heterozygosity have distinct prognostic value for testicular germ cell tumor recurrence. Cancer Biol Ther 2004; 3:1152-8. (Pubitemid 41350999)
37. Richiardi L, Bellocco R, Adami HO, Torrång A, Barlow L, Hakulinen T, et al. Testicular cancer incidence in eight northern European countries: secular and recent trends. Cancer Epidemiol Biomarkers Prev 2004; 13:2157-66.
38. Pettersson A, Akre O, Richiardi L, Ekbom A, Kaijser M. Maternal smoking and the epidemic of testicular cancer - a nested case-control study. Int J Cancer 2007; 120:2044-6. (Pubitemid 46418386)
39. Strohsnitter WC, Noller KL, Hoover RN, Robboy SJ, Palmer JR, Titus-Ernstoff L, et al. Cancer risk in men exposed in utero to diethylstilbestrol. J Natl Cancer Inst 2001; 93:545-51.
40. Hardell L, van Bavel B, Lindström G, Carlberg M, Dreifaldt AC, Wijkström H, et al. Increased concentrations of polychlorinated biphenyls, hexachlorobenzene and chlordanes in mothers of men with testicular cancer. Environ Health Perspect 2003; 111:930-4.
41. Díez-Torre A, Silván U, De Wever O, Bruyneel E, Mareel M, Aréchaga J. Germinal tumor invasion and the role of the testicular stroma. Int J Dev Biol 2004; 48:545-57. (Pubitemid 39360405)
42. Tovar V, Alsinet C, Villanueva A, Hoshida Y, Chiang DY, Solé M, et al. IGF activation in a molecular subclass of hepatocellular carcinoma and pre-clinical efficacy of IGF-1R blockage. J Hepatol 2010; 52:550-9.
43. Tao Y, Pinzi V, Bourhis J, Deutsch E. Mechanisms of disease: signaling of the insulin-like growth factor 1 receptor pathway - therapeutic perspectives in cancer. Nat Clin Pract Oncol 2007; 4:591-602. 0
44. Zhang D, Samani AA, Brodt P. The role of the IGF-I receptor in the regulation of matrix metalloproteinases, tumor invasion and metastasis. Horm Metab Res 2003; 35:802-8.
45. Lin T, Haskell J, Vinson N, Terracio L. Direct stimulatory effects of insulin-like growth factor-I on Leydig cell steroidogenesis in primary culture. Biochem Biophys Res Commun 1986; 137:950-6. (Pubitemid 16049386)
46. Froment P, Vigier M, Nègre D, Fontaine I, Beghelli J, Cosset FL, et al. Inactivation of the IGF-I receptor gene in primary Sertoli cells highlights the autocrine effects of IGF-I. J Endocrinol 2007; 194:557-68.
47. Li Y, Oral O, Abe K, Eto K, Abé S. The roles of pericystic cells and Sertoli cells in spermatogonial proliferation stimulated by some growth factors in organ culture of newt (Cynops pyrrhogaster) testis. Gen Comp Endocrinol 2008; 159:80-7.
48. Schlueter PJ, Sang X, Duan C, Wood AW. Insulin-like growth factor receptor 1b is required for zebrafish primordial germ cell migration and survival. Dev Biol 2007; 305:377-87.
49. Herpin A, Fischer P, Liedtke D, Kluever N, Neuner C, Raz E, et al. Sequential SDF1a and b-induced mobility guides Medaka PGC migration. Dev Biol 2008; 320:319-27.
50. Gilbert DC, Chandler I, McIntyre A, Goddard NC, Gabe R, Huddart RA, et al. Clinical and biological significance of CXCL12 and CXCR4 expression in adult testes and germ cell tumours of adults and adolescents. J Pathol 2009; 217:94-102.
51. Drescher B, Lauke H, Hartmann M, Davidoff MS, Zumkeller W. Immunohistochemical pattern of insulin-like growth factor (IGF) I, IGF II and IGF binding proteins 1 to 6 in carcinoma in situ of the testis. Mol Pathol 1997; 50:298-303.
52. Huang YH, Chin CC, Ho HN, Chou CK, Shen CN, Kuo HC, et al. Pluripotency of mouse spermatogonial stem cells maintained by IGF-1- dependent pathway. FASEB J 2009; 23:2076-87.
53. Engström W. Effects of insulin-like growth factor binding protein 7 on apoptosis in human teratocarcinoma cells in vitro. Anticancer Res 2010; 30:911-4.
54. Granerus M, Engström W. Effects of fibroblast growth factor 8, fibroblast growth factor 9 and keratinocyte growth factor on multiplication and locomotion in human teratocarcinoma cells in vitro. Anticancer Res 2003; 23:1313-6. (Pubitemid 36754093)
55. Valve E, Penttilä TL, Paranko J, Härkönen P. FGF-8 is expressed during specific phases of rodent oocyte and spermatogonium development. Biochem Biophys Res Commun 1997; 232:173-7. (Pubitemid 27211942)
56. Wu J, Payson RA, Lang JC, Chiu IM. Activation of fibroblast growth factor 8 gene expression in human embryonal carcinoma cells. J Steroid Biochem Mol Biol 1997; 62:1-10.
57. Hiramatsu R, Harikae K, Tsunekawa N, Kurohmaru M, Matsuo I, Kanai Y. FGF signaling directs a center-to-pole expansion of tubulogenesis in mouse testis differentiation. Development 2010; 137:303-12.
58. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010; 141:52-67.
59. Ardi VC, Kupriyanova TA, Deryugina EI, Quigley JP. Human neutrophils uniquely release TIMP-free MMP-9 to provide a potent catalytic stimulator of angiogenesis. Proc Natl Acad Sci USA 2007; 104:20262-7.
60. Hawinkels LJ, Zuidwijk K, Verspaget HW, de Jonge-Muller ES, van Duijn W, Ferreira V, et al. VEGF release by MMP-9 mediated heparan sulphate cleavage induces colorectal cancer angiogenesis. Eur J Cancer 2008; 44:1904-13.
61. Luo Y, Zhou H, Krueger J, Kaplan C, Lee SH, Dolman C, et al. Targeting tumor-associated macrophages as a novel strategy against breast cancer. J Clin Invest 2006; 116:2132-41.
62. Tummalapalli P, Spomar D, Gondi CS, Olivero WC, Gujrati M, Dinh DH, et al. RNAi-mediated abrogation of cathepsin B and MMP-9 gene expression in a malignant meningioma cell line leads to decreased tumor growth, invasion and angiogenesis. Int J Oncol 2007; 31:1039-50.
63. Hoeben E, Van Aelst I, Swinnen JV, Opdenakker G, Verhoeven G. Gelatinase A secretion and its control in peritubular and Sertoli cell cultures: effects of hormones, second messengers and inducers of cytokine production. Mol Cell Endocrinol 1996; 118:37-46. (Pubitemid 26146074)
64. Silván U, Díez-Torre A, Arluzea J, Andrade R, Silió M, Aréchaga J. Hypoxia and pluripotency in embryonic and embryonal carcinoma stem cell biology. Differentiation 2009; 78:159-68.
65. Slongo ML, Zampieri M, Onisto M. Expression of matrix metalloproteases (MMP-2, MT1-MMP) and their tissue inhibitor (TIMP-2) by rat Sertoli cells in culture: implications for spermatogenesis. Biol Chem 2002; 383:235-9.
66. Ulanet DB, Ludwig DL, Kahn CR, Hanahan D. Inaugural Article: Insulin receptor functionally enhances multistage tumor progression and conveys intrinsic resistance to IGF-1R targeted therapy. Proc Natl Acad Sci USA 2010; 107:10791-8.
67. Risau W. Mechanisms of angiogenesis. Nature 1997; 386:671-4.
68. Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol 1995; 11:73-91.
69. Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM, Peer J, et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999; 155:739-52.
70. Mayerhofer A, Bartke A. Developing testicular microvasculature in the golden hamster, Mesocricetus auratus: a model for angiogenesis under physiological conditions. Acta Anat (Basel) 1990; 139:78-85.
71. Silván U, Díez-Torre A, Jiménez-Rojo L, Aréchaga J. Vascularization of testicular germ cell tumors: Evidence from experimental teratocarcinomas. Int J Androl 2010; DOI:10.1111/j.1365-2605.2010. 01068.
72. Samson M, Peale FV Jr, Frantz G, Rioux-Leclercq N, Rajpert-De Meyts E, Ferrara N. Human endocrine gland-derived vascular endothelial growth factor: expression early in development and in Leydig cell tumors suggests roles in normal and pathological testis angiogenesis. J Clin Endocrinol Metab 2004; 89:4078-88. (Pubitemid 39071516)
73. Morrison SJ, Csete M, Groves AK, Melega W, Wold B, Anderson DJ. Culture in reduced levels of oxygen promotes clonogenic sympathoadrenal differentiation by isolated neural crest stem cells. J Neurosci 2000; 20:7370-6.
74. Fujii T, Otsuki T, Moriya T, Sakaguchi H, Kurebayashi J, Yata K, et al. Effect of hypoxia on human seminoma cells. Int J Oncol 2002; 20:955-62.
75. Chen J, Imanaka N, Chen J, Griffin JD. Hypoxia potentiates Notch signaling in breast cancer leading to decreased E-cadherin expression and increased cell migration and invasion. Br J Cancer 2010; 102:351-60.
76. Osinsky S, Zavelevich M, Vaupel P. Tumor hypoxia and malignant progression. Exp Oncol 2009; 31:80-6.
77. Sato T, Iwai M, Sakai T, Sato M, Seiki M, Mori Y, et al. Enhancement of membrane-type 1-matrix metalloproteinase (MT1-MMP) production and sequential activation of progelatinase A on human squamous carcinoma cells co-cultures with human dermal fibroblasts. Br J Cancer 1999; 80:1137-43.
78. Schmelz HU, Port M, Stockinger M, Ruf C, Martinscheck A, Sparwasser C, et al. Testis cancer cells have a genetic determination for a high sensitivity to apoptosis inducing stimuli. Urol Oncol 2010; 28:49-58.
79. di Pietro A, Vries EG, Gietema JA, Spierings DC, de Jong S. Testicular germ cell tumours: the paradigm of chemo-sensitive solid tumours. Int J Biochem Cell Biol 2005; 37:2437-56.
80. Sun J, Zhang Y, Yang M, Zhang Y, Xie Q, Li Z, et al. Hypoxia induces T-cell apoptosis by inhibiting chemokine C receptor 7 expression: the role of adenosine receptor A(2). Cell Mol Immunol 2010; 7:77-82.
81. Wang H, Sung Y, Wang L, Xu CL, Qing Y, Liu B, et al. Hypoxia-Induced Apoptosis in the Bilateral Testes of Rats with Left-Sided Varicocele: A New Way to Think about Varicocele. J Androl 2009; [Epub ahead of print].
82. Piret JP, Cosse JP, Ninane N, Raes M, Michiels C. Hypoxia protects HepG2 cells against etoposide-induced apoptosis via a HIF-1-independent pathway. Exp Cell Res 2006; 312:2908-20.
83. Kinoshita M, Johnson DL, Shatney CH, Lee YL, Mochizuki H. Cancer cells surviving hypoxia obtain hypoxia resistance and maintain anti-apoptotic potential under reoxygenation. Int J Cancer 2001; 91:322-6. (Pubitemid 32049625)
84. Josefsen D, Ous S, Høie J, Stenwig AE, Fosså SD. Salvage treatment in male patients with germ cell tumours. Br J Cancer 1993; 67:568-72.
85. Lin Q, Yun Z. Impact of the hypoxic tumor microenvironment on the regulation of cancer stem cell characteristics. Cancer Biol Ther 2010; 9:5-12.
86. Rajpert-De Meyts E. Developmental model for the pathogenesis of testicular carcinoma in situ: genetic and environmental aspects. Hum Reprod Update 2006; 12:303-23.