The spermatogonial stem cell niche in testicular germ cell tumors

International Journal of Developmental Biology

Volumn 57, Issue 2-4, 2013, Pages 185-195

  Silván, Unai ^a   Díez Torre, Alejandro ^b   Moreno, Pablo ^a   Arluzea, Jon ^a,b   Andrade, Ricardo ^b   Silió, Margarita ^a   Aréchaga, Juan ^a,b  

^a Laboratory of Stem Cells   (Spain)

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

Author keywords

Cancer stem cell; Embryonal carcinoma; Germ cell tumor; Spermatogonia; Teratocarcinoma; Testis

Indexed keywords

CELL ADHESION MOLECULE; GROWTH FACTOR;

ARTICLE; BASEMENT MEMBRANE; EUROPE; EXTRACELLULAR MATRIX; GERM CELL TUMOR; HUMAN; MECHANICAL STRESS; MICROENVIRONMENT; NONHUMAN; NORTH AMERICA; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL NICHE; TESTIS TUMOR; TUMOR GROWTH; TUMOR INVASION; VASCULARIZATION;

ANIMALS; CELL DIFFERENTIATION; GERM CELLS; HUMANS; MALE; NEOPLASMS, GERM CELL AND EMBRYONAL; SPERMATOGENESIS; STEM CELL NICHE; TESTICULAR NEOPLASMS;

EID: 84880072670     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.130068ja     Document Type: Article

References (85)

1. ARÉCHAGA J (1993). On the boundary between development and neoplasia. An interview with Professor G. Barry Pierce. Int J Dev Biol 37: 5-16.
2. BARTOLINI, F., and GUNDERSEN, G.G. (2006). Generation of noncentrosomal microtubule arrays. J Cell Sci 119: 4155-4163.
3. BASCIANI, S., MARIANI, S., ARIZZI, M., ULISSE, S., RUCCI, N., JANNINI, E.A., DELLA ROCCA, C., MANICONE, A., CARANI, C., SPERA, G., and GNESSI, L. (2002). Expression of platelet-derived growth factor-A (PDGF-A), PDGF-B, and PDGF receptor-alpha and-beta during human testicular development and disease. J Clin Endocrinol Metab 87: 2310-2319.
4. BATISTATOU, A., SCOPA, C.D., RAVAZOULA, P., NAKANISHI, Y., PESCHOS, D., AGNANTIS, N.J., HIROHASHI, S., and CHARALABOPOULOS, K.A. (2005). In-volvement of dysadherin and E-cadherin in the development of testicular tumours. Br J Cancer 93: 1382-1387.
5. BLAGOEV, K.B. (2011). Organ aging and susceptibility to cancer may be related to the geometry of the stem cell niche. Proc Natl Acad Sci USA 108: 19216-19221.
6. BLOCH, W., FORSBERG, E., LENTINI, S., BRAKEBUSH, C., MARTIN, K., KRELL, H.W., WEIDLE, U.H., ADDICKS, K., and FÄSSLER, R. (1997). b1 integrin is es-sential for teratoma growth and angiogenesis J Cell Biol 139: 265-278.
7. BONAFÈ, M., STORCI, G., and FRANCESCHI, C. (2012). Inflamm-aging of the stem cell niche: breast cancer as a paradigmatic example: breakdown of the multi-shell cytokine network fuels cancer in aged people. Bioessays 34: 40-49.
8. BREMMER, F., HEMMERLEIN, B., STRAUSS, A., BURFEIND, P., THELEN, P., RADZUN, H.J., and BEHNES, C.L. (2012). N-cadherin expression in malignant germ cell tumours of the testis. BMC Clin Pathol 12: 19.
9. CAVEL, O., SHOMRON, O., SHABTAY, A., VITAL, J., TREJO-LEIDER, L., WEIZ-MAN, N., KRELIN, Y., FONG, Y., WONG, R.J., AMIT, M., and GIL, Z. (2012). Endoneurial Macrophages Induce Perineural Invasion of Pancreatic Cancer Cells by Secretion of GDNF and Activation of RET Tyrosine Kinase Receptor. Cancer Res 72: 5733-5743.
10. CHEVALIER, N., BARLIER, A., ROCHE, C., MOGRABI, B., CAMPARO, P., DEV-OUASSOUXS-HISHEBORAN, M., MICHIELS, J.F., NEBOUT, M., CHEVALLIER, D., BENAHMED, M., ENJALBERT, A., and FÉNICHEL, P. (2010). RET gene mutations are not involved in the origin of human testicular seminoma. Int J Androl 33: 848-852.
11. CHOWDHURY, F., NA, S., LI, D., POH, Y.C., TANAKA, T.S., WANG, F., and WANG, N. (2010). Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat Mater 9: 82-88.
12. CLIFFORD, A., LOWELL, M.D., and TANYA, N.M. (2012). Overview-studying integrins in vivo. Methods Mol Biol 757: 369-397.
13. CONIGLIO, S.J., EUGENIN, E., DOBRENIS, K., STANLEY, E.R., WEST, B.L., SY-MONS, M.H., and SEGALL, J.E. (2012). Microglial stimulation of glioblastoma invasion involves epidermal growth factor receptor (EGFR) and colony stimulating factor 1 receptor (CSF-1R) signaling. Mol Med 18: 519-527.
14. CONDEELIS, J., and POLLARD, J.W. (2006). Macrophages: obligate partners for tumor cell migration, invasion and metastasis. Cell 124: 263-266.
15. COLPAERT, C.G., VERMEULEN, P.B., FOX, S.B., HARRIS, A.L., DIRIX, L.Y., and VAN MARCK, E.A. (2003). The presence of a fibrotic focus in invasive breast carcinoma correlates with the expression of carbonic anhydrase IX and is a marker of hypoxia and poor prognosis. Breast Cancer Res Treat 81: 137-147.
16. COLUCCI-GUYON, E., PORTIER, M.M., DUNIA, I., PAULIN, D., POURNIN, S., and BABINET, C. (1994). Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79: 679-694.
17. CONBOY, I.M., CONBOY, M.J., WAGERS, A.J., GIRMA, E.R., WEISSMAN, I.L., and RANDO, T.A. (2005). Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433: 760-764.
18. CORREA, L.M., NAKAI, M., STRANDGAARD, C.S., HESS, R.A., and MILLER, M.G. (2002). Microtubules of the mouse testis exhibit differential sensitivity to the microtubule disruptors Carbendazim and colchicine. Toxicol Sci 69: 175-182.
19. DÍEZ-TORRE, A., SILVÁN, U., DE WEVER, O., BRUYNEEL, E., MAREEL, M., and ARÉCHAGA, J. (2004). Germinal tumor invasion and the role of the testicular stroma. Int J Dev Biol 48: 682-690.
20. DÍEZ-TORRE, A., SILVÁN, U., DÍAZ-NÚÑEZ, M., and ARÉCHAGA, J. (2010). The role of microenvironment in testicular germ cell tumors. Cancer Biol Ther 10: 529-536.
21. DÍEZ-TORRE, A., SILVÁN, U., MORENO, P., GUMUCIO, J., and ARÉCHAGA, J. (2011). Peritubular myoid cell-derived factors and its potential role in the progres-sion of testicular germ cell tumours. Int J Androl 34: e252-264.
22. DRESCHER, B., LAUKE, H., HARTMANN, M., DAVIDOFF, M.S., and ZUMKELLER, W. (1997). 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 50: 298-303.
23. ENGLER, A.J., SEN, S., SWEENEY, H.L., and DISCHER, D.E. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
24. FERRANTI, F., MUCIACCIA, B., RICCI, G., DOVERE, L., CANIPARI, R., MAGLIOCCA, F., STEFANINI, M., CATIZONE, A., and VICINI, E. (2012). Glial cell line-derived neurotrophic factor promotes invasive behaviour in testicular seminoma cells. Int J Androl 35:758-768.
25. FRANKE, W.W., GRUND, C., and SCHMID, E. (1979). Intermediate-sized filaments present in Sertoli cells are of the vimentin type. Eur J Cell Biol 19: 269-275.
26. FROMENT, P., VIGIER, M., NEGRE, D., FONTAINE, I., BEGHELLI, J., COSSET, F.L., HOLZENBERGER, M., and DURAND, P. (2007). Inactivation of the IGF-I receptor gene in primary Sertoli cells highlights the autocrine effects of IGF-I. J Endocrinol 194: 557-568.
27. FUJIMOTO, H., SANGAI, T., ISHII, G., IKEHARA, A., NAGASHIMA, T., MIYAZAKI, M., and OCHIAI, A. (2009). Stromal MCP-1 in mammary tumors induces tumor-associated macrophage infiltration and contributes to tumor progression. Int J Cancer 125: 1276-1284.
28. FURUTA, A., FUNAHASHI, H., SAWAI, H., SATO, M., OKADA, Y., TAKEYAMA, H., and MANABE, T. (2007). The relationship between GDNF and integrins in human colorectal cancer cell activity. Hepatogastroenterology 54: 1398-1402.
29. HOEI-HANSEN, C.E., RAJPERT-DE MEYTS, E., DAUGAARD, G., and SKAKKE-BAEK, N.E. (2005). Carcinoma in situ testis, the progenitor of testicular germ cell tumours: a clinical review. Ann Oncol 16: 863-868.
30. HUANG, Y.H., CHIN, C.C., HO, H.N., CHOU, C.K., SHEN, C.N., KUO, H.C., WU, T.J., WU, Y.C., HUNG, Y.C., CHANG, C.C., and LING, T.Y. (2009). Pluripotency of mouse spermatogonial stem cells maintained by IGF-1-dependent pathway. FASEB J 23: 2076-2087.
31. HUANG, H., NAKAYAMA, Y., QIN, K., YAMAMOTO, K., ANDO, J., YAMASHITA, J., ITOH, H., KANDA, K., YAKU, H., OKAMOTO, Y., and NEMOTO, Y. (2005). Dif-ferentiation from embryonic stem cells to vascular wall cells under in vitro pulsatile flow loading. J Artif Organs 8: 110-118.
32. JIA, D., ENTERSZ, I., BUTLER C., and FOTY R.A. (2012). Fibronectin matrix-mediated cohesion suppresses invasion of prostate cancer cells. BMC Cancer 12: 94.
33. JODELE, S., BLAVIER, L., YOON, J.M., and DECLERCK, Y.A. (2006). Modifying the soil to affect the seed: role of stromal-derived matrix metalloproteinases in cancer progression. Cancer Metastasis Rev 25: 35-43.
34. KANATSU-SHINOHARA, M., INOUE, K., OGONUKI, N., MIKI, H., and YOSHIDA, S. (2007). Leukemia inhibitory factor enhances formation of germ cell colonies in neonatal mouse testis culture. Biol Reprod 76: 55-62.
35. KANATSU-SHINOHARA, M., TAKEHASHI, M., TAKASHIMA, S., LEE, J., MORIMOTO, H., CHUMA, S., RADUCANU, A., NAKATSUJI, N., FÄSSLER, R., and SHINO-HARA, T. (2008). Homing of mouse spermatogonial stem cells to germline niche depends on beta1-integrin. Cell Stem Cell 3: 533-542.
36. KERBEL, R.S. (2008). Tumor angiogenesis. N Engl J Med 358: 2039-2049.
37. KUBOTA, H., AVARBOCK, M.R., and BRINSTER, R.L. (2004). Growth factors es-sential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci USA 101: 16489-16494.
38. LE BRAS, G.F., TAUBENSLAG, K.J., and ANDL, C.D. (2012). The regulation of cell-cell adhesion during epithelial-mesenchymal transition, motility and tumor progression. Cell Adh Migr 6: 365-373.
39. LECKBAND, D., and SIVASANKAR, S. (2012). Cadherin recognition and adhesion. Curr Opin Cell Biol 24: 620-627.
40. LEE, J., KANATSU-SHINOHARA, M., INOUE, K., OGONUKI, N., and MIKI, H. (2007). Akt mediates self-renewal division of mouse spermatogonial stem cells. Development 134: 1853-1859.
41. LOSINNO, A.D., MORALES, A., FERNÁNDEZ, D., and LOPEZ, L.A. (2012). Peritu-bular myoid cells from rat seminiferous tubules contain actin and myosin filaments distributed in two independent layers. Biol Reprod 86: 1-8.
42. LUPIAÑEZ, D.G., REAL, F.M., DADHICH, R.K., CARMONA, F.D., BURGOS, M., BARRIONUEVO, F.J., and JIMÉNEZ, R. (2012). Pattern and density of vascu-larization in mammalian testes, ovaries, and ovotestes. J Exp Zool B Mol Dev Evo 318: 170-181.
43. MACKAY, S., and SMITH, R.A. (2007). Effects of growth factors on testicular mor-phogenesis. Int Rev Cytol 260: 113-173.
44. MAGGI, M., BARNI, T., ORLANDO, C., FANTONI, G., FINETTI, G., VANNELLI, G.B., MANCINA, R., GLORIA, L., BONACCORSI, L., YANAGISAWA, M., and FORTI, G. (1995). Endothelin-1 and its receptors in human testis. J Androl 16: 213-224.
45. MAGNANTI, M., GISMONDI, A., GANDINI, O., ROSSI, F.M., MICHETTI, P.M., SAN-TIEMMA, V., and MORRONE, S. (2001). Integrin Pattern and Effect on Contraction in Cultured Testicular Peritubular Myoid Cells. AJRI 45: 21-27.
46. MAZUMDAR, J., DONDETI, V., and SIMON, M.C. (2009). Hypoxia-inducible factors in stem cells and cancer. J Cell Mol Med 13: 4319-4328.
47. McCABE, N.P., DE, S., VASANJI, A., BRAINARD, J., and BYZOVA, T.V. (2007). Prostate cancer specific integrin avb3 modulates bone metastatic growth and tissue remodeling. Oncogene 26: 6238-6243.
48. MENG, X., LINDAHL, M., HYVÖNEN, M.E., PARVINEN, M., and DE ROOIJ, D.G. (2000). Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287: 1489-1493.
49. MIETTINEN, M., VIRTANEN, I., and TALERMAN, A. (1985). Intermediate filament proteins in human testis and testicular germ-cell tumors. Am J Pathol 120: 402-410.
50. MULLANEY, B.P., and SKINNER, M.K. (1992). Basic fibroblast growth factor (bFGF) gene expression and protein production during pubertal development of the semi-niferous tubule: folliclestimulating hormone-induced Sertoli cell bFGF expression. Endocrinology 131: 2928-2934.
51. NAGANO, M., RYU, B.Y., BRINSTER, C.J., AVARBOCK, M.R., and BRINSTER, R.L. (2003). Maintenance of mouse male germ line stem cells in vitro. Biol Reprod 68: 2207-2214.
52. NAKAYAMA, H., ENZAN, H., MIYAZAKI, E., NARUSE, K., KIYOKU, H., and HIROI, M. (1998). The role of myofibroblasts at the tumor border of invasive colorectal adenocarcinomas. Jpn J Clin Oncol 28: 615-620.
53. NAKAGAWA, T., SHARMA, M., NABESHIMA, Y., BRAUN, R.E., and YOSHIDA, S. (2010). Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science 328: 62-67.
54. OATLEY J M and BRINSTER R L (2008) Regulation of spermatogonial stem cell self-renewal in mammals. Ann Rev Cell Dev Biol 24: 263-286
55. OATLEY J M and BRINSTER R L (2012) The germline stem cell niche unit in mam-malian testes. Physiol Rev 92: 577-595
56. OATLEY, J.M., OATLEY, M.J., AVARBOCK, M.R., TOBIAS, J.W., and BRINSTER, R.L. (2009). Colony stimulating factor 1 is an extrinsic stimulator of mouse sper-matogonial stem cell self-renewal. Development 136: 1191-1199.
57. OLSEN, A.L., BLOOMER, S.A., CHAN, E.P., GAÇA, M.D., GEORGES, P.C., SACKEY, B., UEMURA, M., JANMEY, P.A., and WELLS, R.G. (2011). Hepatic stellate cells require a stiff environment for myofibroblastic differentiation. Am J Physiol Gastrointest Liver Physiol 301: 110-118.
58. OOSTERHUIS J W and LOOIJENGA L H (2005) Testicular germ-cell tumors in a broader perspective. Nat Rev Cancer 5: 210-222.
59. PARANKO, J., KALLAJOKI, M., PELLINIEMI, L.J., LEHTO, V.P., and VIRTANEN, I. (1986). Transient coexpression of cytokeratin and vimentin in differentiating rat Sertoli cells. Dev Biol 117: 35-44.
60. PYONTECK, S.M., GADEA, B.B., WANG, H.W., GOCHEVA, V., HUNTER, K.E., TANG, L.H., and JOYCE, J.A. (2012). Deficiency of the macrophage growth factor CSF-1 disrupts pancreatic neuroendocrine tumor development. Oncogene 31: 1459-1467.
61. RAJPERT-DE MEYTS, E. (2006). Developmental model for the pathogenesis of testicular carcinoma in situ: genetic and environmental aspects. Hum Reprod Update 12: 303-323.
62. SCHELL, C., ALBRECHT, M., MAYER, C., SCHWARZER, J.U., FRUNGIERI, M.B., and MAYERHOFER, A. (2008). Exploring human testicular peritubular cells: identification of secretory products and regulation by tumor necrosis factor-alpha. Endocrinology 149: 1678-1686.
63. SCHOFIELD, R. (1978). The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4: 7-25.
64. SCHLUETER, P.J., SANG, X., DUAN, C., and WOOD, A.W. (2007). Insulin-like growth factor receptor 1b is required for zebrafish primordial germ cell migration and survival. Dev Biol 305: 377-387.
65. SILVAN, U., and ARECHAGA, J. (2012). Anatomical basis for cell transplantation into mouse seminiferous tubules. Reproduction 144: 385-392.
66. SILVÁN, U., DÍEZ-TORRE, A., ANDRADE, R., ARLUZEA, J., SILIÓ, M., and ARÉ-CHAGA, J. (2011). Embryonic stem cell transplantation into seminiferous tubules: a model for the study of invasive germ cell tumors of the testis. Cell Transplant 20: 637-642.
67. SILVÁN, U., ARLUCEA, J., ANDRADE, R., DÍEZ-TORRE, A., SILIÓ, M., KONERD-ING, M.A., and ARÉCHAGA, J. (2009a). Angiogenesis and vascular network of teratocarcinoma from embryonic stem cell transplant into seminiferous tubules. Br J Cancer 101: 64-70.
68. SILVÁN, U., DÍEZ-TORRE, A., ARLUZEA, J., ANDRADE, R., SILIÓ, M., and ARÉ-CHAGA, J. (2009b). Hypoxia and pluripotency in embryonic and embryonal carcinoma stem cell biology. Differentiation 78: 159-168.
69. SILVÁN, U., DÍEZ-TORRE, A., JIMÉNEZ-ROJO, L., and ARÉCHAGA, J. (2010). Vascularization of testicular germ cell tumours: evidence from experimental teratocarcinomas. Int J Androl 33: 765-774.
70. SPINNLER, K., KÖHN, F.M., SCHWARZER, U., and MAYERHOFER, A. (2010). Glial cell line-derived neurotrophic factor is constitutively produced by human testicular peritubular cells and may contribute to the spermatogonial stem cell niche in man. Hum Reprod 25: 2181-2187.
71. SU, C.M., LU, D.Y., HSU, C.J., CHEN, H.T., HUANG, C.Y., YANG, W.H., SU, Y.C., YANG, S.N., FONG, Y.C., TSENG, W.P., and TANG, C.H. (2009). Glial cell-derived neurotrophic factor increases migration of human chondrosarcoma cells via ERK and NF-kappaB pathways. J Cell Physiol 220: 499-507.
72. SUZUKI, H., SADA, A., YOSHIDA, S., and SAGA, Y. (2009). The heterogeneity of spermatogonia is revealed by their topology and expression of marker proteins including the germ cell-specific proteins Nanos2 and Nanos3. Dev Biol 336: 222-231.
73. TADOKORO, Y., YOMOGIDA, K., OHTA, H., TOHDA, A., and NISHIMUNE, Y. (2002). Homeostatic regulation of germinal stem cell proliferation by the GDNF/FSH pathway. Mech Dev 113: 29-39.
74. TAVERNA, D., and HYNES, R.O. (2001). Reduced blood vessel formation and tumor growth in alpha5-integrin-negative teratocarcinomas and embryoid bodies. Cancer Res 61: 5255-5261.
75. TIMMER, A., OOSTERHUIS, J.W., SCHRAFFORDT KOOPS, H., SLEIJFER, D.T., SZABO, B.G., and TIMENS, W. (1994). The tumor microenvironment: possible role of integrins and the extracellular matrix in tumor biological behaviour of intratubular germ cell neoplasia and testicular seminomas. Am J Pathol 144: 1035-1044.
76. VANNELLI, B.G., BARNI, T., ORLANDO, C., NATALI, A., SERIO, M., and BALBONI, G.C. (1988). Insulin-like growth factor-I (IGF-I) and IGF-I receptor in human testis: an immunohistochemical study. Fertil Steril 49: 666-669.
77. VAUPEL, P. (2008). Hypoxia and aggressive tumor phenotype: implications for therapy and prognosis. Oncologist 13: 21-26.
78. VOGL, A.W. (1988). Changes in the distribution of microtubules in rat Sertoli cells during spermatogenesis. Anat Rec 222: 34-41.
79. VOGL, A.W., VAID, K.S., and GUTTMAN, J.A. (2008). The Sertoli cell cytoskeleton. Adv Exp Med Biol 636: 186-211.
80. WAN, G., and TOO, H.P. (2010). A specific isoform of glial cell line-derived neuro-trophic factor family receptor alpha 1 regulates RhoA expression and glioma cell migration. J Neurochem 115: 759-70.
81. WANG, H., RIHA, G.M., YAN, S., LI, M., CHAI, H., YANG, H., YAO, Q., and CHEN, C. (2005). Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol 25: 1817-1823.
82. WILSON, M.J., BOWLES, J., and KOOPMAN, P. (2006). The matricellular protein SPARC is internalized in Sertoli, Leydig, and germ cells during testis differentia-tion. Mol Reprod Dev 73: 531-539.
83. WONG, C.W, DYE, D.E., and COOMBE, D.R. (2012). The role of immunoglobulin superfamily cell adhesion molecules in cancer metastasis. Int J Cell Biol 2012: 340296 (doi: 10.1155/2012/340296).
84. WROBEL, K.H., SCHILLING, E., and ZWACK, M. (1986). Postnatal development of the connexion between tubulus seminiferous and tubulus rectus in the bovine testis. Cell Tissue Res 246: 387-400.
85. YOSHIDA, S., SUKENO, M., and NABESHIMA, Y. (2007). A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 317: 1722-1726.