Inactivation of Numb and Numblike in spermatogonial stem cells by cell-permeant Cre recombinase

Differentiation

Volumn 78, Issue 2-3, 2009, Pages 131-136

  Grisanti, Laura ^a   Corallini, Serena ^a   Fera, Stefania ^a   Muciaccia, Barbara ^a   Stefanini, Mario ^a   Witke, Walter ^b   Vicini, Elena ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

Author keywords

Cre recombinase; Germ cell transplantation; Numb; Spermatogenesis; Spermatogonial stem cells; Stem cells

Indexed keywords

ADAPTOR PROTEIN; CRE RECOMBINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL ISOLATION; CELL RENEWAL; CELL TRANSPLANTATION; CONTROLLED STUDY; DEATH; EX VIVO STUDY; GAMETE; GENE FUNCTION; GENE INACTIVATION; GENE LOSS; GENE MUTATION; GENETIC TRANSDUCTION; GERM LINE; HOMOZYGOSITY; MAMMAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; RODENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPERMATID; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL; TESTIS; WILD TYPE;

ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; GENE SILENCING; INTEGRASES; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; SPERMATOGONIA; STEM CELLS; TESTIS; TRANSDUCTION, GENETIC;

MAMMALIA; MUS; RODENTIA;

EID: 69949168424     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2009.05.005     Document Type: Article

References (55)

1. Aponte P.M., Soda T., Teerds K.J., Mizrak S.C., van de Kant H.J., and de Rooij D.G. Propagation of bovine spermatogonial stem cells in vitro. Reproduction 136 (2008) 543-557
2. Berdnik D., Torok T., Gonzalez-Gaitan M., and Knoblich J.A. The endocytic protein alpha-adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev. Cell 3 (2002) 221-231
3. Boitani C., Palombi F., and Stefanini M. Influence of Sertoli cell products upon the in vitro survival of isolated spermatocytes and spermatids. Cell Biol. Int. Rep. 7 (1983) 383-393
4. Brinster R.L. Germline stem cell transplantation and transgenesis. Science 296 (2002) 2174-2176
5. Buaas F.W., Kirsh A.L., Sharma M., McLean D.J., Morris J.L., Griswold M.D., de Rooij D.G., and Braun R.E. Plzf is required in adult male germ cells for stem cell self-renewal. Nat. Genet. 36 (2004) 647-652
6. Chen C., Ouyang W., Grigura V., Zhou Q., Carnes K., Lim H., Zhao G.Q., Arber S., Kurpios N., Murphy T.L., Cheng A.M., Hassell J.A., Chandrashekar V., Hofmann M.C., Hess R.A., and Murphy K.M. ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 436 (2005) 1030-1034
7. Colaluca I.N., Tosoni D., Nuciforo P., Senic-Matuglia F., Galimberti V., Viale G., Pece S., and Di Fiore P.P. Numb controls p53 tumour suppressor activity. Nature 451 (2008) 76-80
8. Conrad S., Renninger M., Hennenlotter J., Wiesner T., Just L., Bonin M., Aicher W., Buhring H.J., Mattheus U., Mack A., Wagner H.J., Minger S., Matzkies M., Reppel M., Hescheler J., Sievert K.D., Stenzl A., and Skutella T. Generation of pluripotent stem cells from adult human testis. Nature 456 (2008) 344-349
9. Corallini S., Fera S., Grisanti L., Falciatori I., Muciaccia B., Stefanini M., and Vicini E. Expression of the adaptor protein m-Numb in mouse male germ cells. Reproduction 132 (2006) 887-897
10. Costoya J.A., Hobbs R.M., Barna M., Cattoretti G., Manova K., Sukhwani M., Orwig K.E., Wolgemuth D.J., and Pandolfi P.P. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat. Genet. 36 (2004) 653-659
11. de Rooij D.G., and Russell L.D. All you wanted to know about spermatogonia but were afraid to ask. J. Androl. 21 (2000) 776-798
12. Di Marcotullio L., Ferretti E., Greco A., De Smaele E., Po A., Sico M.A., Alimandi M., Giannini G., Maroder M., Screpanti I., and Gulino A. Numb is a suppressor of Hedgehog signalling and targets Gli1 for itch-dependent ubiquitination. Nat. Cell Biol. 8 (2006) 1415-1423
13. Falciatori I., Borsellino G., Haliassos N., Boitani C., Corallini S., Battistini L., Bernardi G., Stefanini M., and Vicini E. Identification and enrichment of spermatogonial stem cells displaying side-population phenotype in immature mouse testis. FASEB J. 18 (2004) 376-378
14. French M.B., Koch U., Shaye R.E., McGill M.A., Dho S.E., Guidos C.J., and McGlade C.J. Transgenic expression of Numb inhibits notch signaling in immature thymocytes but does not alter T cell fate specification. J. Immunol. 168 (2002) 3173-3180
15. Friedrich G., and Soriano P. Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5 (1991) 1513-1523
16. Gallardo T., Shirley L., John G., and Castrillon D.H. Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre. Genesis 45 (2007) 413-417
17. Guan K., Nayernia K., Maier L.S., Wagner S., Dressel R., Lee J.H., Nolte J., Wolf F., Li M., Engel W., and Hasenfuss G. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440 (2006) 1199-1203
18. Guo M., Jan L.Y., and Jan Y.N. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17 (1996) 27-41
19. Hamra F.K., Gatlin J., Chapman K.M., Grellhesl D.M., Garcia J.V., Hammer R.E., and Garbers D.L. Production of transgenic rats by lentiviral transduction of male germ-line stem cells. Proc. Natl. Acad. Sci. USA 99 (2002) 14931-14936
20. Honaramooz A., Megee S., Zeng W., Destrempes M.M., Overton S.A., Luo J., Galantino-Homer H., Modelski M., Chen F., Blash S., Melican D.T., Gavin W.G., Ayres S., Yang F., Wang P.J., Echelard Y., and Dobrinski I. Adeno-associated virus (AAV)-mediated transduction of male germ line stem cells results in transgene transmission after germ cell transplantation. FASEB J. 22 (2008) 374-382
21. Huang E.J., Li H., Tang A.A., Wiggins A.K., Neve R.L., Zhong W., Jan L.Y., and Jan Y.N. Targeted deletion of Numb and Numblike in sensory neurons reveals their essential functions in axon arborization. Genes Dev. 19 (2005) 138-151
22. Kanatsu-Shinohara M., Ikawa M., Takehashi M., Ogonuki N., Miki H., Inoue K., Kazuki Y., Lee J., Toyokuni S., Oshimura M., Ogura A., and Shinohara T. Production of knockout mice by random or targeted mutagenesis in spermatogonial stem cells. Proc. Natl. Acad. Sci. USA 103 (2006) 8018-8023
23. Kanatsu-Shinohara M., Inoue K., Lee J., Yoshimoto M., Ogonuki N., Miki H., Baba S., Kato T., Kazuki Y., Toyokuni S., Toyoshima M., Niwa O., Oshimura M., Heike T., Nakahata T., Ishino F., Ogura A., and Shinohara T. Generation of pluripotent stem cells from neonatal mouse testis. Cell 119 (2004) 1001-1012
24. Kanatsu-Shinohara M., Miki H., Inoue K., Ogonuki N., Toyokuni S., Ogura A., and Shinohara T. Long-term culture of mouse male germline stem cells under serum-or feeder-free conditions. Biol. Reprod. 72 (2005) 985-991
25. Knoblich J.A., Jan L.Y., and Jan Y.N. Asymmetric segregation of Numb and Prospero during cell division. Nature 377 (1995) 624-627
26. Kossack, N., Meneses, J., Shefi, S., Nguyen, H.N., Chavez, S., Nicholas, C., Gromoll, J., Turek, P.J., Reijo-Pera, R.A., 2008. Isolation and characterization of pluripotent human spermatogonial stem cell-derived cells. Stem Cells.
27. Kubota H., and Brinster R.L. Technology insight: in vitro culture of spermatogonial stem cells and their potential therapeutic uses. Nat. Clin. Pract. Endocrinol. Metab. 2 (2006) 99-108
28. Kyriazis G.A., Wei Z., Vandermey M., Jo D.G., Xin O., Mattson M.P., and Chan S.L. Numb endocytic adapter proteins regulate the transport and processing of the amyloid precursor protein in an isoform-dependent manner: implications for Alzheimer disease pathogenesis. J. Biol. Chem. 283 (2008) 25492-25502
29. Le Borgne R., Bardin A., and Schweisguth F. The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 132 (2005) 1751-1762
30. Lomeli H., Ramos-Mejia V., Gertsenstein M., Lobe C.G., and Nagy A. Targeted insertion of Cre recombinase into the TNAP gene: excision in primordial germ cells. Genesis 26 (2000) 116-117
31. Meng X., Lindahl M., Hyvonen M.E., Parvinen M., de Rooij D.G., Hess M.W., Raatikainen-Ahokas A., Sainio K., Rauvala H., Lakso M., Pichel J.G., Westphal H., Saarma M., and Sariola H. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287 (2000) 1489-1493
32. Morena A.R., Boitani C., Pesce M., De Felici M., and Stefanini M. Isolation of highly purified type A spermatogonia from prepubertal rat testis. J. Androl. 17 (1996) 708-717
33. Nagano M., Brinster C.J., Orwig K.E., Ryu B.Y., Avarbock M.R., and Brinster R.L. Transgenic mice produced by retroviral transduction of male germ-line stem cells. Proc. Natl. Acad. Sci. USA 98 (2001) 13090-13095
34. Nishimura T., Fukata Y., Kato K., Yamaguchi T., Matsuura Y., Kamiguchi H., and Kaibuchi K. CRMP-2 regulates polarized Numb-mediated endocytosis for axon growth. Nat. Cell Biol. 5 (2003) 819-826
35. Nishimura T., and Kaibuchi K. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 13 (2007) 15-28
36. Nolden L., Edenhofer F., Haupt S., Koch P., Wunderlich F.T., Siemen H., and Brustle O. Site-specific recombination in human embryonic stem cells induced by cell-permeant Cre recombinase. Nat. Methods 3 (2006) 461-467
37. O'Gorman S., Dagenais N.A., Qian M., and Marchuk Y. Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc. Natl. Acad. Sci. USA 94 (1997) 14602-14607
38. Pece S., Serresi M., Santolini E., Capra M., Hulleman E., Galimberti V., Zurrida S., Maisonneuve P., Viale G., and Di Fiore P.P. Loss of negative regulation by Numb over Notch is relevant to human breast carcinogenesis. J. Cell Biol. 167 (2004) 215-221
39. Peitz M., Pfannkuche K., Rajewsky K., and Edenhofer F. Ability of the hydrophobic FGF and basic TAT peptides to promote cellular uptake of recombinant Cre recombinase: a tool for efficient genetic engineering of mammalian genomes. Proc. Natl. Acad. Sci. USA 99 (2002) 4489-4494
40. Petersen P.H., Zou K., Hwang J.K., Jan Y.N., and Zhong W. Progenitor cell maintenance requires Numb and Numblike during mouse neurogenesis. Nature 419 (2002) 929-934
41. In: Russell L.D., Ettlin R.A., Sinha Hikim A.P., and Clegg E.D. (Eds). Histological and Histopathological Evaluation of the Testis (1999), Chache River Press, Clearwater
42. Sadate-Ngatchou P.I., Payne C.J., Dearth A.T., and Braun R.E. Cre recombinase activity specific to postnatal, premeiotic male germ cells in transgenic mice. Genesis 46 (2008) 738-742
43. Seandel M., James D., Shmelkov S.V., Falciatori I., Kim J., Chavala S., Scherr D.S., Zhang F., Torres R., Gale N.W., Yancopoulos G.D., Murphy A., Valenzuela D.M., Hobbs R.M., Pandolfi P.P., and Rafii S. Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 449 (2007) 346-350
44. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21 (1999) 70-71
45. Spana E.P., and Doe C.Q. Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17 (1996) 21-26
46. Spana E.P., Kopczynski C., Goodman C.S., and Doe C.Q. Asymmetric localization of Numb autonomously determines sibling neuron identity in the Drosophila CNS. Development 121 (1995) 3489-3494
47. Takehashi M., Kanatsu-Shinohara M., Inoue K., Ogonuki N., Miki H., Toyokuni S., Ogura A., and Shinohara T. Adenovirus-mediated gene delivery into mouse spermatogonial stem cells. Proc. Natl. Acad. Sci. USA 104 (2007) 2596-2601
48. Uemura T., Shepherd S., Ackerman L., Jan L.Y., and Jan Y.N. Numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 58 (1989) 349-360
49. Wan S., Cato A.M., and Skaer H. Multiple signalling pathways establish cell fate and cell number in Drosophila malpighian tubules. Dev. Biol. 217 (2000) 153-165
50. Wilson A., Ardiet D.L., Saner C., Vilain N., Beermann F., Aguet M., Macdonald H.R., and Zilian O. Normal hemopoiesis and lymphopoiesis in the combined absence of Numb and Numblike. J. Immunol. 178 (2007) 6746-6751
51. Yoshida S., Takakura A., Ohbo K., Abe K., Wakabayashi J., Yamamoto M., Suda T., and Nabeshima Y. Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev. Biol. 269 (2004) 447-458
52. Zhang X., Ebata K.T., and Nagano M.C. Genetic analysis of the clonal origin of regenerating mouse spermatogenesis following transplantation. Biol. Reprod. 69 (2003) 1872-1878
53. Zhong W., Feder J.N., Jiang M.M., Jan L.Y., and Jan Y.N. Asymmetric localization of a mammalian Numb homolog during mouse cortical neurogenesis. Neuron 17 (1996) 43-53
54. Zhong W., Jiang M.M., Schonemann M.D., Meneses J.J., Pedersen R.A., Jan L.Y., and Jan Y.N. Mouse Numb is an essential gene involved in cortical neurogenesis. Proc. Natl. Acad. Sci. USA 97 (2000) 6844-6849
55. Zilian O., Saner C., Hagedorn L., Lee H.Y., Sauberli E., Suter U., Sommer L., and Aguet M. Multiple roles of mouse Numb in tuning developmental cell fates. Curr. Biol. 11 (2001) 494-501