The roles of testicular c-kit positive cells in de novo morphogenesis of testis

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Zhang, Man ^a,b   Zhou, Hai ^a,c   Zheng, Chunxing ^d   Xiao, Jun ^a   Zuo, Erwei ^a,e   Liu, Wujuan ^a   Xie, Da ^g   Shi, Yufang ^d   Wu, Chunlian ^c   Wang, Hongyan ^a   Li, Dangsheng ^a,g   Li, Jinsong ^a,f  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c CHINA WEST NORMAL UNIVERSITY   (China)

^d SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^e GUANGXI UNIVERSITY   (China)

^f SHANGHAITECH UNIVERSITY   (China)

^g Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; DIFFERENTIATION ANTIGEN; MONOCYTE-MACROPHAGE DIFFERENTIATION ANTIGEN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; STEM CELL FACTOR RECEPTOR;

ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HETEROTOPIC TRANSPLANTATION; MACROPHAGE; MALE; METABOLISM; MORPHOGENESIS; MOUSE; NUDE MOUSE; SPERMATID; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS;

ANIMALS; ANTIGENS, DIFFERENTIATION; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, NUDE; MORPHOGENESIS; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; SPERMATIDS; SPERMATOGENESIS; SPERMATOGONIA; TESTIS; TRANSPLANTATION, HETEROTOPIC;

EID: 84905457579     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep05936     Document Type: Article

References (53)

1. Lennartsson, J. & Ronnstrand, L. Stem cell factor receptor/c-Kit: from basic science to clinical implications. Physiol Rev 92, 1619-1649 (2012).
2. Ronnstrand, L. Signal transduction via the stem cell factor receptor/c-Kit. Cell Mol Life Sci 61, 2535-2548 (2004). (Pubitemid 39586516)
3. Orlic, D., Fischer, R., Nishikawa, S., Nienhuis, A. W. & Bodine, D. M. Purification and characterization of heterogeneous pluripotent hematopoietic stem cell populations expressing high levels of c-kit receptor. Blood 82, 762-770 (1993). (Pubitemid 23221654)
4. Ogawa, M. et al. Expression and function of c-kit in hemopoietic progenitor cells. J Exp Med 174, 63-71 (1991).
5. Bearzi, C. et al. Human cardiac stem cells. Proc Nat Acad Sci USA 104, 14068-14073 (2007). (Pubitemid 350003336)
6. Tallini, Y. N. et al. c-kit expression identifies cardiovascular precursors in the neonatal heart. Proc Nat Acad Sci USA 106, 1808-1813 (2009).
7. Beltrami, A. P. et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114, 763-776 (2003). (Pubitemid 37186770)
8. Kajstura, J. et al. Evidence for human lung stem cells. N Engl Med 364, 1795-1806 (2011).
9. Loffredo, F. S., Steinhauser, M. L., Gannon, J. & Lee, R. T. Bone marrow-derived cell therapy stimulates endogenous cardiomyocyte progenitors and promotes cardiac repair. Cell stem cell 8, 389-398 (2011).
10. Mauduit, C., Hamamah, S. & Benahmed, M. Stem cell factor/c-kit system in spermatogenesis. Hum Reprod Update 5, 535-545 (1999). (Pubitemid 29512140)
11. Sette, C., Dolci, S., Geremia, R. & Rossi, P. The role of stem cell factor and of alternative c-kit gene products in the establishment, maintenance and function of germ cells. Int J Dev Biol 44, 599-608 (2000).
12. Zhang, L. et al. c-kit and its related genes in spermatogonial differentiation. Spermatogenesis 1, 186-194 (2011).
13. Orr-Urtreger, A. et al. Developmental expression of c-kit, a proto-oncogene encoded by the W locus. Development 109, 911-923 (1990).
14. Schrans-Stassen, B. H., van de Kant, H. J., de Rooij, D. G. & van Pelt, A. M. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 140, 5894-5900 (1999). (Pubitemid 30645378)
15. Yoshinaga, K. et al. Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 113, 689-699 (1991).
16. Shinohara, T., Orwig, K. E., Avarbock, M. R. & Brinster, R. L. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc Nat Acad Sci USA 97, 8346-8351 (2000). (Pubitemid 30639675)
17. Kubota, H., Avarbock, M. R. & Brinster, R. L. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Nat Acad Sci USA 100, 6487-6492 (2003). (Pubitemid 36666608)
18. Shinohara, T., Avarbock, M. R. & Brinster, R. L. beta1-and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Nat Acad Sci USA 96, 5504-5509 (1999). (Pubitemid 29234647)
19. Dores, C., Alpaugh, W. & Dobrinski, I. From in vitro culture to in vivo models to study testis development and spermatogenesis. Cell Tissue Res 349, 691-702 (2012).
20. Kita, K. et al. Production of functional spermatids from mouse germline stem cells in ectopically reconstituted seminiferous tubules. Biol Reprod 76, 211-217 (2007). (Pubitemid 46219335)
21. Honaramooz, A., Megee, S. O., Rathi, R. & Dobrinski, I. Building a testis: formation of functional testis tissue after transplantation of isolated porcine (Sus scrofa) testis cells. Biol Reprod 76, 43-47 (2007). (Pubitemid 46013446)
22. Arregui, L. et al. Xenografting of sheep testis tissue and isolated cells as a model for preservation of genetic material from endangered ungulates. Reproduction 136, 85-93 (2008). (Pubitemid 351984722)
23. Bastos, H. et al. Flow cytometric characterization of viable meiotic and postmeiotic cells by Hoechst 33342 in mouse spermatogenesis. Cytometry A 65, 40-49 (2005). (Pubitemid 40604985)
24. Yang, H. et al. Generation of genetically modified mice by oocyte injection of androgenetic haploid embryonic stem cells. Cell 149, 605-617 (2012).
25. Oatley, J. M. & Brinster, R. L. The germline stem cell niche unit in mammalian testes. Physiol Rev 92, 577-595 (2012).
26. Kanatsu-Shinohara, M., Toyokuni, S. & Shinohara, T. CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod 70, 70-75 (2004). (Pubitemid 38063552)
27. Hofmann, M. C., Braydich-Stolle, L. & Dym, M. Isolation of male germ-line stem cells; influence of GDNF. Dev Biol 279, 114-124 (2005). (Pubitemid 40222173)
28. Meng, X. et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287, 1489-1493 (2000). (Pubitemid 30127143)
29. Kanatsu-Shinohara, M. et al. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod 69, 612-616 (2003). (Pubitemid 36885967)
30. Gnessi, L. et al. Leydig cell loss and spermatogenic arrest in platelet-derived growth factor (PDGF)-A-deficient mice. J Cell Biol 149, 1019-1026 (2000).
31. Barroca, V. et al. Mouse differentiating spermatogonia can generate germinal stem cells in vivo. Nat Cell Biol 11, 190-196 (2009).
32. Manova, K., Nocka, K., Besmer, P. & Bachvarova, R.F.Gonadal expression ofc-kit encoded at the W locus of the mouse. Development 110, 1057-1069 (1990). (Pubitemid 120009477)
33. Griswold, S. L. & Behringer, R. R. Fetal Leydig cell origin and development. Sex Dev 3, 1-15 (2009).
34. Cohen, P. E., Nishimura, K., Zhu, L. & Pollard, J. W. Macrophages: important accessory cells for reproductive function. J Leukoc Biol 66, 765-772 (1999). (Pubitemid 29532038)
35. Winnall, W. R. & Hedger, M. P. Phenotypic and functional heterogeneity of the testicular macrophage population: a new regulatory model. J Reprod Immunol 97, 147-158 (2013).
36. Hume, D. A., Halpin, D., Charlton, H. & Gordon, S. The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: macrophages of endocrine organs. Proc Nat Acad Sci USA 81, 4174-4177 (1984). (Pubitemid 14054543)
37. Itoh, M., Xie, Q., Miyamoto, K. & Takeuchi, Y. F4/80-positive cells rapidly accumulate around tubuli recti and rete testis between 3 and 4 weeks of age in the mouse: an immunohistochemical study. Am J Reprod Immunol 42, 321-326 (1999). (Pubitemid 29502165)
38. Zhang, X., Goncalves, R. & Mosser, D. M. The isolation and characterization of murine macrophages. Curr Protoc Immunol Chapter 14, Unit 14 11 (2008).
39. Mosser, D. M. & Edwards, J. P. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8, 958-969 (2008).
40. Fadok, V. A. et al. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 101, 890-898 (1998). (Pubitemid 28096086)
41. DeFalco, T., Takahashi, S. & Capel, B. Two distinct origins for Leydig cell progenitors in the fetal testis. Dev Biol 352, 14-26 (2011).
42. Ren, G. et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell stem cell 2, 141-150, doi:10.1016/j.stem.2007.11.014 (2008). (Pubitemid 351181031)
43. Hutson, J. C., Garner, C. W. & Doris, P. A. Purification and characterization of a lipophilic factor from testicular macrophages that stimulates testosterone production by Leydig cells. J Androl 17, 502-508 (1996). (Pubitemid 26403610)
44. Hayashi, K., Ohta, H., Kurimoto, K., Aramaki, S. & Saitou, M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146, 519-532 (2011).
45. Hayashi, K. et al. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 338, 971-975 (2012).
46. Rodriguez-Sosa, J. R. & Dobrinski, I. Recent developments in testis tissue xenografting. Reproduction 138, 187-194 (2009).
47. Gassei, K., Schlatt, S. & Ehmcke, J. De novo morphogenesis of seminiferous tubules from dissociated immature rat testicular cells in xenografts. J Androl 27, 611-618 (2006). (Pubitemid 44126275)
48. Hadley, M. A., Byers, S. W., Suarez-Quian, C. A., Kleinman, H. K. & Dym, M. Extracellular matrix regulates Sertoli cell differentiation, testicular cord formation, and germ cell development in vitro. J Cell Biol 101, 1511-1522 (1985). (Pubitemid 16234178)
49. Hedger, M.P.Macrophages and the immune responsiveness ofthe testis.JReprod Immunol 57, 19-34 (2002). (Pubitemid 35245737)
50. Bergh, A., Damber, J. E. & van Rooijen, N. Liposome-mediated macrophage depletion: an experimental approach to study the role of testicular macrophages in the rat. J Endocrinol 136, 407-413 (1993). (Pubitemid 23142206)
51. Gaytan, F. et al. In vivo manipulation (depletion versus activation) of testicular macrophages: central and local effects. J Endocrinol 150, 57-65 (1996). (Pubitemid 26232634)
52. Cohen, P. E., Chisholm, O., Arceci, R. J., Stanley, E. R. & Pollard, J. W. Absence of colony-stimulating factor-1 in osteopetrotic (csfmop/csfmop) mice results in male fertility defects. Biol Reprod 55, 310-317 (1996). (Pubitemid 26301140)
53. Hutson, J. C. Physiologic interactions between macrophages and Leydig cells. Exp Biol Med 231, 1-7 (2006). (Pubitemid 43063972)