Gene expression profiling of rat spermatogonia and Sertoli cells reveals signaling pathways from stem cells to niche and testicular cancer cells to surrounding stroma

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Ryser, Stephan ^a,f   Glauser, Dominique ^b   Vigier, Michelle ^c   Zhang, Yong Q ^a   Tachini, Philippe ^d   Schlegel, Werner ^b   Durand, Philippe ^c,e   Irminger Finger, Irmgard ^a  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b Fondation pour Recherches Medicales   (Switzerland)

^c HÔPITAL DEBROUSSE   (France)

^d EDEL Therapeutics SA   (Switzerland)

^e UNIVERSITÉ LYON 1   (France)

^f LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CANCER CELL; CELL ADHESION; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL PROLIFERATION; CONTROLLED STUDY; DNA MICROARRAY; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC REGULATION; IN SITU HYBRIDIZATION; INTRACELLULAR SIGNALING; MALE; MICROENVIRONMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA PURIFICATION; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL NICHE; STROMA; TESTIS CANCER; ANIMAL; CLUSTER ANALYSIS; GENETICS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; TESTIS TUMOR;

MAMMALIA; RATTUS;

ANIMALS; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERTOLI CELLS; SIGNAL TRANSDUCTION; SPERMATOGONIA; STEM CELLS; TESTICULAR NEOPLASMS;

EID: 78651302321     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-29     Document Type: Article

References (94)

1. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 2004, 116(6):769-778. 10.1016/S0092-8674(04)00255-7, 15035980.
2. Li L, Xie T. Stem cell niche: structure and function. Annu Rev Cell Dev Biol 2005, 21:605-631. 10.1146/annurev.cellbio.21.012704.131525, 16212509.
3. Scadden DT. The stem-cell niche as an entity of action. Nature 2006, 441(7097):1075-1079. 10.1038/nature04957, 16810242.
4. Wong MD, Jin Z, Xie T. Molecular mechanisms of germline stem cell regulation. Annu Rev Genet 2005, 39:173-195. 10.1146/annurev.genet.39.073003.105855, 16285857.
5. de Rooij DG. Stem cells in the testis. Int J Exp Pathol 1998, 79(2):67-80. 10.1046/j.1365-2613.1998.00057.x, 9709376.
6. de Rooij DG. Proliferation and differentiation of spermatogonial stem cells. Reproduction 2001, 121(3):347-354. 10.1530/rep.0.1210347, 11226060.
7. de Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000, 21(6):776-798.
8. Kierszenbaum AL. Mammalian spermatogenesis in vivo and in vitro: a partnership of spermatogenic and somatic cell lineages. Endocr Rev 1994, 15(1):116-134.
9. Yan W. Molecular mechanisms of spermatogonial fate control: lesson from gene knockouts. Biol Reprod 2006, 75(3):487.
10. Yoshida S, Sukeno M, Nakagawa T, Ohbo K, Nagamatsu G, Suda T, Nabeshima Y. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development 2006, 133(8):1495-1505. 10.1242/dev.02316, 16540512.
11. Nakagawa T, Nabeshima Y, Yoshida S. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 2007, 12(2):195-206. 10.1016/j.devcel.2007.01.002, 17276338.
12. Buageaw A, Sukhwani M, Ben-Yehudah A, Ehmcke J, Rawe VY, Pholpramool C, Orwig KE, Schlatt S. GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biol Reprod 2005, 73(5):1011-1016. 10.1095/biolreprod.105.043810, 16014811.
13. Yoshida S, Nabeshima Y, Nakagawa T. Stem cell heterogeneity: actual and potential stem cell compartments in mouse spermatogenesis. Ann N Y Acad Sci 2007, 1120:47-58. 10.1196/annals.1411.003, 17905929.
14. Griswold MD. Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 1995, 52(2):211-216. 10.1095/biolreprod52.2.211, 7711190.
15. Griswold MD. The central role of Sertoli cells in spermatogenesis. Semin Cell Dev Biol 1998, 9(4):411-416. 10.1006/scdb.1998.0203, 9813187.
16. Brinster CJ, Ryu BY, Avarbock MR, Karagenc L, Brinster RL, Orwig KE. Restoration of fertility by germ cell transplantation requires effective recipient preparation. Biol Reprod 2003, 69(2):412-420. 10.1095/biolreprod.103.016519, 12672656.
17. Ogawa T, Dobrinski I, Brinster RL. Recipient preparation is critical for spermatogonial transplantation in the rat. Tissue Cell 1999, 31(5):461-472. 10.1054/tice.1999.0060, 10612257.
18. Shinohara T, Orwig KE, Avarbock MR, Brinster RL. Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility. Proc Natl Acad Sci USA 2001, 98(11):6186-6191. 10.1073/pnas.111158198, 33443, 11371640.
19. Ryu BY, Orwig KE, Avarbock MR, Brinster RL. Stem cell and niche development in the postnatal rat testis. Dev Biol 2003, 263(2):253-263. 10.1016/j.ydbio.2003.07.010, 14597200.
20. McLean DJ, Friel PJ, Johnston DS, Griswold MD. Characterization of spermatogonial stem cell maturation and differentiation in neonatal mice. Biol Reprod 2003, 69(6):2085-2091. 10.1095/biolreprod.103.017020, 12954735.
21. Chalmel F, Rolland AD, Niederhauser-Wiederkehr C, Chung SS, Demougin P, Gattiker A, Moore J, Patard JJ, Wolgemuth DJ, Jegou B, et al. The conserved transcriptome in human and rodent male gametogenesis. Proc Natl Acad Sci USA 2007, 104(20):8346-8351. 10.1073/pnas.0701883104, 1864911, 17483452.
22. Schlecht U, Demougin P, Koch R, Hermida L, Wiederkehr C, Descombes P, Pineau C, Jegou B, Primig M. Expression profiling of mammalian male meiosis and gametogenesis identifies novel candidate genes for roles in the regulation of fertility. Mol Biol Cell 2004, 15(3):1031-1043. 10.1091/mbc.E03-10-0762, 363067, 14718556.
23. Hamra FK, Schultz N, Chapman KM, Grellhesl DM, Cronkhite JT, Hammer RE, Garbers DL. Defining the spermatogonial stem cell. Dev Biol 2004, 269(2):393-410. 10.1016/j.ydbio.2004.01.027, 15110708.
24. Schultz N, Hamra FK, Garbers DL. A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc Natl Acad Sci USA 2003, 100(21):12201-12206. 10.1073/pnas.1635054100, 218736, 14526100.
25. Shima JE, McLean DJ, McCarrey JR, Griswold MD. The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod 2004, 71(1):319-330. 10.1095/biolreprod.103.026880, 15028632.
26. McLean DJ, Friel PJ, Pouchnik D, Griswold MD. Oligonucleotide microarray analysis of gene expression in follicle-stimulating hormone-treated rat Sertoli cells. Mol Endocrinol 2002, 16(12):2780-2792. 10.1210/me.2002-0059, 12456799.
27. Oatley JM, Avarbock MR, Telaranta AI, Fearon DT, Brinster RL. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci USA 2006, 103(25):9524-9529. 10.1073/pnas.0603332103, 1480440, 16740658.
28. Oosterhuis JW, Looijenga LH. Testicular germ-cell tumours in a broader perspective. Nat Rev Cancer 2005, 5(3):210-222. 10.1038/nrc1568, 15738984.
29. Rajpert-De Meyts E, Bartkova J, Samson M, Hoei-Hansen CE, Frydelund-Larsen L, Bartek J, Skakkebaek NE. The emerging phenotype of the testicular carcinoma in situ germ cell. APMIS 2003, 111(1):267-278. discussion 278-269.
30. Clark AT. The stem cell identity of testicular cancer. Stem Cell Rev 2007, 3(1):49-59. 10.1007/s12015-007-0002-x, 17873381.
31. Boitani C, Politi MG, Menna T. Spermatogonial cell proliferation in organ culture of immature rat testis. Biol Reprod 1993, 48(4):761-767. 10.1095/biolreprod48.4.761, 8485240.
32. Clermont Y, Perey B. Quantitative study of the cell population of the seminiferous tubules in immature rats. Am J Anat 1957, 100(2):241-267. 10.1002/aja.1001000205, 13435229.
33. Dym M, Jia MC, Dirami G, Price JM, Rabin SJ, Mocchetti I, Ravindranath N. Expression of c-kit receptor and its autophosphorylation in immature rat type A spermatogonia. Biol Reprod 1995, 52(1):8-19. 10.1095/biolreprod52.1.8, 7536046.
34. Jahnukainen K, Chrysis D, Hou M, Parvinen M, Eksborg S, Soder O. Increased apoptosis occurring during the first wave of spermatogenesis is stage-specific and primarily affects midpachytene spermatocytes in the rat testis. Biol Reprod 2004, 70(2):290-296. 10.1095/biolreprod.103.018390, 14522836.
35. Jarvis S, Elliott DJ, Morgan D, Winston R, Readhead C. Molecular markers for the assessment of postnatal male germ cell development in the mouse. Hum Reprod 2005, 20(1):108-116. 10.1093/humrep/deh565, 15539445.
36. Brehm R, Steger K. Regulation of Sertoli cell and germ cell differentation. Adv Anat Embryol Cell Biol 2005, 181:1-93. full_text, 16281455.
37. Fijak M, Meinhardt A. The testis in immune privilege. Immunol Rev 2006, 213:66-81. 10.1111/j.1600-065X.2006.00438.x, 16972897.
38. Dettin L, Ravindranath N, Hofmann MC, Dym M. Morphological characterization of the spermatogonial subtypes in the neonatal mouse testis. Biol Reprod 2003, 69(5):1565-1571. 10.1095/biolreprod.103.016394, 12855601.
39. Fouchecourt S, Godet M, Sabido O, Durand P. Glial cell-line-derived neurotropic factor and its receptors are expressed by germinal and somatic cells of the rat testis. J Endocrinol 2006, 190(1):59-71. 10.1677/joe.1.06699, 16837611.
40. Seandel M, James D, Shmelkov SV, Falciatori I, Kim J, Chavala S, Scherr DS, Zhang F, Torres R, Gale NW, et al. Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 2007, 449(7160):346-350. 10.1038/nature06129, 2935199, 17882221.
41. Braydich-Stolle L, Kostereva N, Dym M, Hofmann MC. Role of Src family kinases and N-Myc in spermatogonial stem cell proliferation. Dev Biol 2007, 304(1):34-45. 10.1016/j.ydbio.2006.12.013, 2077853, 17222400.
42. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, Bernstein BE, Jaenisch R. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 2007, 448(7151):318-324. 10.1038/nature05944, 17554336.
43. Munsie M, Schlatt S, deKretser DM, Loveland KL. Expression of stem cell factor in the postnatal rat testis. Mol Reprod Dev 1997, 47(1):19-25. 10.1002/(SICI)1098-2795(199705)47:1<19::AID-MRD3>3.0.CO;2-T, 9110310.
44. McConnell MJ, Chevallier N, Berkofsky-Fessler W, Giltnane JM, Malani RB, Staudt LM, Licht JD. Growth suppression by acute promyelocytic leukemia-associated protein PLZF is mediated by repression of c-myc expression. Mol Cell Biol 2003, 23(24):9375-9388. 10.1128/MCB.23.24.9375-9388.2003, 309637, 14645547.
45. Dadoune JP. New insights into male gametogenesis: what about the spermatogonial stem cell niche?. Folia Histochem Cytobiol 2007, 45(3):141-147.
46. Wang PJ, Pan J. The role of spermatogonially expressed germ cell-specific genes in mammalian meiosis. Chromosome Res 2007, 15(5):623-632. 10.1007/s10577-007-1141-2, 17674150.
47. Li C, Scott DA, Hatch E, Tian X, Mansour SL. Dusp6 (Mkp3) is a negative feedback regulator of FGF-stimulated ERK signaling during mouse development. Development 2007, 134(1):167-176. 10.1242/dev.02701, 2424197, 17164422.
48. Wadham C, Gamble JR, Vadas MA, Khew-Goodall Y. The protein tyrosine phosphatase Pez is a major phosphatase of adherens junctions and dephosphorylates beta-catenin. Mol Biol Cell 2003, 14(6):2520-2529. 10.1091/mbc.E02-09-0577, 194899, 12808048.
49. Brady-Kalnay SM, Mourton T, Nixon JP, Pietz GE, Kinch M, Chen H, Brackenbury R, Rimm DL, Del Vecchio RL, Tonks NK. Dynamic interaction of PTPmu with multiple cadherins in vivo. J Cell Biol 1998, 141(1):287-296. 10.1083/jcb.141.1.287, 2132733, 9531566.
50. Woodings JA, Sharp SJ, Machesky LM. MIM-B, a putative metastasis suppressor protein, binds to actin and to protein tyrosine phosphatase delta. Biochem J 2003, 371(Pt 2):463-471. 10.1042/BJ20021962, 1223315, 12570871.
51. Sorio C, Melotti P, D'Arcangelo D, Mendrola J, Calabretta B, Croce CM, Huebner K. Receptor protein tyrosine phosphatase gamma, Ptp gamma, regulates hematopoietic differentiation. Blood 1997, 90(1):49-57.
52. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 2002, 298(5593):597-600. 10.1126/science.1072530, 12228720.
53. Shinohara T, Avarbock MR, Brinster RL. beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci USA 1999, 96(10):5504-5509. 10.1073/pnas.96.10.5504, 21889, 10318913.
54. Tokuda M, Kadokawa Y, Kurahashi H, Marunouchi T. CDH1 is a specific marker for undifferentiated spermatogonia in mouse testes. Biol Reprod 2007, 76(1):130-141. 10.1095/biolreprod.106.053181, 17035642.
55. Closa D, Motoo Y, Iovanna JL. Pancreatitis-associated protein: from a lectin to an anti-inflammatory cytokine. World J Gastroenterol 2007, 13(2):170-174.
56. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000, 287(5457):1489-1493. 10.1126/science.287.5457.1489, 10688798.
57. Wu J, Jester WF, Orth JM. Short-type PB-cadherin promotes survival of gonocytes and activates JAK-STAT signalling. Dev Biol 2005, 284(2):437-450. 10.1016/j.ydbio.2005.05.042, 16038895.
58. Orth JM, Jester WF. NCAM mediates adhesion between gonocytes and Sertoli cells in cocultures from testes of neonatal rats. J Androl 1995, 16(5):389-399.
59. Dar A, Goichberg P, Shinder V, Kalinkovich A, Kollet O, Netzer N, Margalit R, Zsak M, Nagler A, Hardan I, et al. Chemokine receptor CXCR4-dependent internalization and resecretion of functional chemokine SDF-1 by bone marrow endothelial and stromal cells. Nat Immunol 2005, 6(10):1038-1046. 10.1038/ni1251, 16170318.
60. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006, 25(6):977-988. 10.1016/j.immuni.2006.10.016, 17174120.
61. Nikolova G, Strilic B, Lammert E. The vascular niche and its basement membrane. Trends Cell Biol 2007, 17(1):19-25. 10.1016/j.tcb.2006.11.005, 17129728.
62. Bagnato A, Spinella F. Emerging role of endothelin-1 in tumor angiogenesis. Trends Endocrinol Metab 2003, 14(1):44-50. 10.1016/S1043-2760(02)00010-3, 12475611.
63. Kristensen DM, Sonne SB, Ottesen AM, Perrett RM, Nielsen JE, Almstrup K, Skakkebaek NE, Leffers H, Meyts ER. Origin of pluripotent germ cell tumours: the role of microenvironment during embryonic development. Mol Cell Endocrinol 2008, 288(1-2):111-118. 10.1016/j.mce.2008.02.018, 18420341.
64. Brehm R, Ruttinger C, Fischer P, Gashaw I, Winterhager E, Kliesch S, Bohle RM, Steger K, Bergmann M. Transition from preinvasive carcinoma in situ to seminoma is accompanied by a reduction of connexin 43 expression in Sertoli cells and germ cells. Neoplasia 2006, 8(6):499-509. 10.1593/neo.05847, 1601470, 16820096.
65. Brehm R, Marks A, Rey R, Kliesch S, Bergmann M, Steger K. Altered expression of connexins 26 and 43 in Sertoli cells in seminiferous tubules infiltrated with carcinoma-in-situ or seminoma. J Pathol 2002, 197(5):647-653. 10.1002/path.1140, 12210085.
66. Kliesch S, Behre HM, Hertle L, Bergmann M. Alteration of Sertoli cell differentiation in the presence of carcinoma in situ in human testes. J Urol 1998, 160(5):1894-1898. 10.1016/S0022-5347(01)62439-X, 9783981.
67. Fink C, Weigel R, Hembes T, Lauke-Wettwer H, Kliesch S, Bergmann M, Brehm RH. Altered expression of ZO-1 and ZO-2 in Sertoli cells and loss of blood-testis barrier integrity in testicular carcinoma in situ. Neoplasia 2006, 8(12):1019-1027. 10.1593/neo.06559, 1783719, 17217619.
68. Davidoff MS, Middendorff R, Koeva Y, Pusch W, Jezek D, Muller D. Glial cell line-derived neurotrophic factor (GDNF) and its receptors GFRalpha-1 and GFRalpha-2 in the human testis. Ital J Anat Embryol 2001, 106(2 Suppl 2):173-180.
69. Almstrup K, Hoei-Hansen CE, Wirkner U, Blake J, Schwager C, Ansorge W, Nielsen JE, Skakkebaek NE, Rajpert-De Meyts E, Leffers H. Embryonic stem cell-like features of testicular carcinoma in situ revealed by genome-wide gene expression profiling. Cancer Res 2004, 64(14):4736-4743. 10.1158/0008-5472.CAN-04-0679, 15256440.
70. Hoei-Hansen CE, Nielsen JE, Almstrup K, Hansen MA, Skakkebaek NE, Rajpert-DeMeyts E, Leffers H. Identification of genes differentially expressed in testes containing carcinoma in situ. Mol Hum Reprod 2004, 10(6):423-431. 10.1093/molehr/gah059, 15123780.
71. Korkola JE, Houldsworth J, Dobrzynski D, Olshen AB, Reuter VE, Bosl GJ, Chaganti RS. Gene expression-based classification of nonseminomatous male germ cell tumors. Oncogene 2005, 24(32):5101-5107. 10.1038/sj.onc.1208694, 15870693.
72. Korkola JE, Houldsworth J, Chadalavada RS, Olshen AB, Dobrzynski D, Reuter VE, Bosl GJ, Chaganti RS. Down-regulation 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(2):820-827. 10.1158/0008-5472.CAN-05-2445, 16424014.
73. Skotheim RI, Lind GE, Monni O, Nesland JM, Abeler VM, Fossa SD, Duale N, Brunborg G, Kallioniemi O, Andrews PW, et al. Differentiation of human embryonal carcinomas in vitro and in vivo reveals expression profiles relevant to normal development. Cancer Res 2005, 65(13):5588-5598. 10.1158/0008-5472.CAN-05-0153, 15994931.
74. Sperger JM, Chen X, Draper JS, Antosiewicz JE, Chon CH, Jones SB, Brooks JD, Andrews PW, Brown PO, Thomson JA. Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors. Proc Natl Acad Sci USA 2003, 100(23):13350-13355. 10.1073/pnas.2235735100, 263817, 14595015.
75. Yamada S, Kohu K, Ishii T, Ishidoya S, Hiramatsu M, Kanto S, Fukuzaki A, Adachi Y, Endoh M, Moriya T, et al. Gene expression profiling identifies a set of transcripts that are up-regulated inhuman testicular seminoma. DNA Res 2004, 11(5):335-344. 10.1093/dnares/11.5.335, 15747581.
76. Almstrup K, Ottesen AM, Sonne SB, Hoei-Hansen CE, Leffers H, Rajpert-De Meyts E, Skakkebaek NE. Genomic and gene expression signature of the pre-invasive testicular carcinoma in situ. Cell Tissue Res 2005, 322(1):159-165. 10.1007/s00441-005-1084-x, 15846514.
77. Houldsworth J, Reuter V, Bosl GJ, Chaganti RS. Aberrant expression of cyclin D2 is an early event in human male germ cell tumorigenesis. Cell Growth Differ 1997, 8(3):293-299.
78. Bartkova J, Rajpert-de Meyts E, Skakkebaek NE, Bartek J. D-type cyclins in adult human testis and testicular cancer: relation to cell type, proliferation, differentiation, and malignancy. J Pathol 1999, 187(5):573-581. 10.1002/(SICI)1096-9896(199904)187:5<573::AID-PATH289>3.0.CO;2-H, 10398124.
79. Chen XD, Dusevich V, Feng JQ, Manolagas SC, Jilka RL. Extracellular matrix made by bone marrow cells facilitates expansion of marrow-derived mesenchymal progenitor cells and prevents their differentiation into osteoblasts. J Bone Miner Res 2007, 22(12):1943-1956. 10.1359/jbmr.070725, 17680726.
80. Yao Y, Shahbazian A, Bostrom KI. Proline and gamma-carboxylated glutamate residues in matrix Gla protein are critical for binding of bone morphogenetic protein-4. Circ Res 2008, 102(9):1065-1074. 10.1161/CIRCRESAHA.107.166124, 18369157.
81. Capurro MI, Xu P, Shi W, Li F, Jia A, Filmus J. Glypican-3 inhibits Hedgehog signaling during development by competing with patched for Hedgehog binding. Dev Cell 2008, 14(5):700-711. 10.1016/j.devcel.2008.03.006, 18477453.
82. Yoshida S, Sukeno M, Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007, 317(5845):1722-1726. 10.1126/science.1144885, 17823316.
83. Karnoub AE, Weinberg RA. Chemokine networks and breast cancer metastasis. Breast Dis 2006, 26:75-85.
84. Bucci LR, Brock WA, Johnson TS, Meistrich ML. Isolation and biochemical studies of enriched populations of spermatogonia and early primary spermatocytes from rat testes. Biol Reprod 1986, 34(1):195-206. 10.1095/biolreprod34.1.195, 3955136.
85. Onoda M, Djakiew D, Papadopoulos V. Pachytene spermatocytes regulate the secretion of Sertoli cell protein(s) which stimulate Leydig cell steroidogenesis. Mol Cell Endocrinol 1991, 77(1-3):207-216. 10.1016/0303-7207(91)90076-5, 1816003.
86. Weiss M, Vigier M, Hue D, Perrard-Sapori MH, Marret C, Avallet O, Durand P. Pre- and postmeiotic expression of male germ cell-specific genes throughout 2-week cocultures of rat germinal and Sertoli cells. Biol Reprod 1997, 57(1):68-76. 10.1095/biolreprod57.1.68, 9209082.
87. Franke WW, Grund C, Schmid E. Intermediate-sized filaments present in Sertoli cells are of the vimentin type. Eur J Cell Biol 1979, 19(3):269-275.
88. Kopecky M, Semecky V, Nachtigal P. Vimentin expression during altered spermatogenesis in rats. Acta Histochem 2005, 107(4):279-289. 10.1016/j.acthis.2005.06.007, 16139876.
89. Suter L, Koch E, Bechter R, Bobadilla M. Three-parameter flow cytometric analysis of rat spermatogenesis. Cytometry 1997, 27(2):161-168. 10.1002/(SICI)1097-0320(19970201)27:2<161::AID-CYTO8>3.0.CO;2-J, 9012383.
90. Li L, Cohen M, Wu J, Sow MH, Nikolic B, Bischof P, Irminger-Finger I. Identification of BARD1 splice-isoforms involved in human trophoblast invasion. Int J Biochem Cell Biol 2007, 39(9):1659-1672. 10.1016/j.biocel.2007.04.018, 17556008.
91. Wu JY, Vlastos AT, Pelte MF, Caligo MA, Bianco A, Krause KH, Laurent GJ, Irminger-Finger I. Aberrant expression of BARD1 in breast and ovarian cancers with poor prognosis. Int J Cancer 2006, 118(5):1215-1226. 10.1002/ijc.21428, 16152612.
92. Hubbell E, Liu WM, Mei R. Robust estimators for expression analysis. Bioinformatics 2002, 18(12):1585-1592. 10.1093/bioinformatics/18.12.1585, 12490442.
93. Ryser S, Tortola S, van Haasteren G, Muda M, Li S, Schlegel W. MAP kinase phosphatase-1 gene transcription in rat neuroendocrine cells is modulated by a calcium-sensitive block to elongation in the first exon. J Biol Chem 2001, 276(36):33319-33327. 10.1074/jbc.M102326200, 11423551.
94. Fujita T, Piuz I, Schlegel W. Transcription elongation factors are involved in programming hormone production in pituitary neuroendocrine GH4C1 cells. Mol Cell Endocrinol 319(1-2):63-70. 10.1016/j.mce.2010.01.020, 20097260.