Growth hormone responsive neural precursor cells reside within the adult mammalian brain

Scientific Reports

Volumn 2, Issue , 2012, Pages

  Blackmore, Daniel G ^a   Reynolds, Brent A ^a,b   Golmohammadi, Mohammad G ^a,c   Large, Beatrice ^a   Aguilar, Roberto M ^d   Haro, Luis ^e   Waters, Michael J ^a   Rietze, Rodney L ^a,f  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF FLORIDA   (United States)

^c ARDABIL UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^f PFIZER GLOBAL RESEARCH AND DEVELOPMENT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH HORMONE; GROWTH HORMONE RECEPTOR;

ANIMAL; ARTICLE; BRAIN; C57BL MOUSE; CYTOLOGY; FEMALE; FLOW CYTOMETRY; MALE; METABOLISM; MOUSE; MOUSE MUTANT; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL;

ANIMALS; BRAIN; FEMALE; FLOW CYTOMETRY; GROWTH HORMONE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL STEM CELLS; NEUROGENESIS; RECEPTORS, SOMATOTROPIN;

EID: 84859768534     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep00250     Document Type: Article

References (57)

1. Reynolds, B. A. & Weiss, S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710 (1992).
2. Morshead, C. M. et al. Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13, 1071-1082 (1994). (Pubitemid 24372126)
3. Ming, G. L. & Song, H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28, 223-250 (2005). (Pubitemid 41098905)
4. Emsley, J. G., Mitchell, B. D., Kempermann, G. & Macklis, J. D. Adult neurogenesis and repair of the adultCNSwith neural progenitors, precursors, and stem cells. Progress in neurobiology 75, 321-341 (2005). (Pubitemid 40733268)
5. Thored, P. et al. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24, 739-747 (2006). (Pubitemid 44464779)
6. Potten, C. S. & Loeffler, M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110, 1001-1020 (1990). (Pubitemid 120009472)
7. Till, J. E. & Mc, C. E. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiation research 14, 213-222 (1961).
8. Doetsch, F., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17, 5046-5061 (1997). (Pubitemid 27263818)
9. Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716 (1999). (Pubitemid 29278045)
10. Kriegstein, A. & Alvarez-Buylla, A. The glial nature of embryonic and adult neural stem cells. Annual review of neuroscience 32, 149-184 (2009).
11. Merkle, F. T., Tramontin, A. D., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci USA 101, 17528-17532 (2004). (Pubitemid 39657437)
12. Garcia, A. D., Doan, N. B., Imura, T., Bush, T. G. & Sofroniew, M. V. GFAPexpressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7, 1233-1241 (2004). (Pubitemid 39426243)
13. Mignone, J. L., Kukekov, V., Chiang, A. S., Steindler, D. & Enikolopov, G. Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 469, 311-324 (2004). (Pubitemid 38140640)
14. Coskun, V. et al. CD1331 neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci USA 105, 1026-1031 (2008). (Pubitemid 351282075)
15. Jackson, E. L. et al. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 51, 187-199 (2006). (Pubitemid 44063617)
16. Chojnacki, A., Mak, G. & Weiss, S. PDGFRalpha expression distinguishes GFAPexpressing neural stem cells from PDGF-responsive neural precursors in the adult periventricular area. J Neurosci 31, 9503-9512 (2011).
17. Blackmore, D. G. & Rietze, R. L. in Heart Development and Regeneration Vol. 2 (eds R. P. Harvey & N. Rosenthal) Ch. 13. 1, 857-877 (Academic Press, 2010).
18. Blau, H. M., Brazelton, T. R. & Weimann, J. M. The evolving concept of a stem cell: entity or function? Cell 105, 829-841 (2001). (Pubitemid 32635085)
19. Golmohammadi, M. G. et al. Comparative analysis of the frequency and distribution of stem and progenitor cells in the adult mouse brain. Stem Cells 26, 979-987 (2008).
20. Reynolds, B. A. & Rietze, R. L. Neural stem cells and neurospheres-re-evaluating the relationship. Nat Methods 2, 333-336 (2005). (Pubitemid 41130977)
21. Louis, S. A. et al. Enumeration of neural stem and progenitor cells in the neural colony forming cell assay. Stem Cells 26, 988-996 (2008).
22. Pluchino, S. et al. Persistent inflammation alters the function of the endogenous brain stem cell compartment. Brain : a journal of neurology 131, 2564-2578 (2008).
23. Azari, H., Louis, S. A., Sharififar, S., Vedam-Mai, V. & Reynolds, B. A. Neuralcolony forming cell assay: an assay to discriminate bona fide neural stem cells from neural progenitor cells. J Vis Exp, (2011).
24. Blackmore, D. G., Golmohammadi, M. G., Large, B., Waters, M. J. & Rietze, R. L. Exercise increases neural stem cell number in a growth hormone-dependent manner, augmenting the regenerative response in aged mice. Stem Cells 27, 2044-2052 (2009).
25. Young, K. M., Fogarty, M., Kessaris, N. & Richardson, W. D. Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J Neurosci 27, 8286-8296 (2007). (Pubitemid 47219615)
26. Ajo, R., Cacicedo, L., Navarro, C. & Sanchez-Franco, F. Growth hormone action on proliferation and differentiation of cerebral cortical cells from fetal rat. Endocrinology 144, 1086-1097 (2003). (Pubitemid 36262875)
27. Scheepens, A. et al. Growth hormone as a neuronal rescue factor during recovery from CNS injury. Neuroscience 104, 677-687 (2001). (Pubitemid 32607421)
28. Noguchi, T. Effects of growth hormone on cerebral development: morphological studies. Horm Res 45, 5-17 (1996). (Pubitemid 26037123)
29. Morisawa, K., Sugisaki, T., Kanamatsu, T., Aoki, T. & Noguchi, T. Factors contributing to cerebral hypomyelination in the growth hormone-deficient little mouse. Neurochem Res 14, 173-177 (1989). (Pubitemid 19106900)
30. Zhou, Y. et al. A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor/binding protein gene (the Laron mouse).Proc Natl Acad Sci USA 94, 13215-13220 (1997). (Pubitemid 27518502)
31. Ransome, M. I., Goldshmit, Y., Bartlett, P. F., Waters, M. J. & Turnley, A. M. Comparative analysis of CNS populations in knockout mice with altered growth hormone responsiveness. Eur J Neurosci 19, 2069-2079 (2004). (Pubitemid 38582196)
32. Turnley, A. M., Faux, C. H., Rietze, R. L., Coonan, J. R. & Bartlett, P. F. Suppressor of cytokine signaling 2 regulates neuronal differentiation by inhibiting growth hormone signaling. Nat Neurosci 5, 1155-1162 (2002). (Pubitemid 35247174)
33. Nieves-Martinez, E. et al. Early-onset GH deficiency results in spatial memory impairment in mid-life and is prevented by GH supplementation. J Endocrinol 204, 31-36 (2010).
34. Ramsey, M. M., Weiner, J. L., Moore, T. P., Carter, C. S. & Sonntag, W. E. Growth hormone treatment attenuates age-related changes in hippocampal short-term plasticity and spatial learning. Neuroscience 129, 119-127 (2004). (Pubitemid 39360948)
35. Azcoitia, I. et al. Growth hormone prevents neuronal loss in the aged rat hippocampus. Neurobiology of aging 26, 697-703 (2005). (Pubitemid 40228762)
36. Hojvat, S. et al. Growth hormone (GH), thyroid-stimulating hormone (TSH), and luteinizing hormone (LH)-like peptides in the rodent brain: non-parallel ontogenetic development with pituitary counterparts. Brain Res 256, 427-434 (1982). (Pubitemid 13252019)
37. Gossard, F., Dihl, F., Pelletier, G., Dubois, P. M. & Morel, G. In situ hybridization to rat brain and pituitary gland of growth hormone cDNA. Neurosci Lett 79, 251-256 (1987). (Pubitemid 17124166)
38. Lobie, P. E. et al. Localization and ontogeny of growth hormone receptor gene expression in the central nervous system. Brain Res Dev Brain Res 74, 225-233 (1993). (Pubitemid 23205441)
39. Zhai, Q., Lai, Z., Roos, P. & Nyberg, F. Characterization of growth hormone binding sites in rat brain. Acta Paediatr Suppl 406, 92-95 (1994).
40. Nyberg, F. Growth hormone in the brain: characteristics of specific brain targets for the hormone and their functional significance. Front Neuroendocrinol 21, 330-348 (2000).
41. Pan, W. et al. Permeation of growth hormone across the blood-brain barrier. Endocrinology 146, 4898-4904 (2005). (Pubitemid 41446628)
42. McLenachan, S., Lum, M. G., Waters, M. J. & Turnley, A. M. Growth hormone promotes proliferation of adult neurosphere cultures. Growth Horm IGF Res 19, 212-218 (2009).
43. Pathipati, P. et al. Growth hormone and prolactin regulate human neural stem cell regenerative activity. Neuroscience 190, 409-427 (2011).
44. Corti, S. et al. Isolation and characterization of murine neural stem/progenitor cells based on Prominin-1 expression. Exp Neurol 205, 547-562 (2007). (Pubitemid 46778917)
45. Kee, N., Sivalingam, S., Boonstra, R. & Wojtowicz, J. M. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115, 97-105 (2002). (Pubitemid 34202283)
46. Brown, J. P. et al. Transient expression of doublecortin during adult neurogenesis. The Journal of comparative neurology 467, 1-10 (2003). (Pubitemid 37339753)
47. Gascon, E., Vutskits, L., Jenny, B., Durbec, P. & Kiss, J. Z. PSA-NCAM in postnatally generated immature neurons of the olfactory bulb: a crucial role in regulating p75 expression and cell survival. Development 134, 1181-1190 (2007). (Pubitemid 46630086)
48. Aguilar, R. M. et al. MAP dendrimer elicits antibodies for detecting rat and mouse GH-binding proteins. J Pept Sci 15, 78-88 (2009).
49. Piccirillo, S. G. et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444, 761-765 (2006). (Pubitemid 44949605)
50. Deleyrolle, L. P. et al. Determination of somatic and cancer stem cell self-renewing symmetric division rate using sphere assays. PLoS One 6, e15844 (2011).
51. Doetsch, F., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci USA 96, 11619-11624 (1999). (Pubitemid 29487430)
52. Marshall, G. P., 2nd, Scott, E. W., Zheng, T., Laywell, E. D. & Steindler, D. A. Ionizing radiation enhances the engraftment of transplanted in vitro-derived multipotent astrocytic stem cells. Stem Cells 23, 1276-1285 (2005). (Pubitemid 41504915)
53. Tada, E., Yang, C., Gobbel, G. T., Lamborn, K. R. & Fike, J. R. Long-term impairment of subependymal repopulation following damage by ionizing irradiation. Exp Neurol 160, 66-77 (1999).
54. Craig, C. G. et al. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16, 2649-2658 (1996). (Pubitemid 26122682)
55. Kornblum, H. I. & Geschwind, D. H. Molecular markers in CNS stem cell research: hitting amoving target. Nature reviews. Neuroscience 2, 843-846 (2001). (Pubitemid 33674067)
56. Rando, T. A. Stem cells, ageing and the quest for immortality. Nature 441, 1080-1086 (2006). (Pubitemid 43990720)
57. Rietze, R., Poulin, P. & Weiss, S. Mitotically active cells that generate neurons and astrocytes are present in multiple regions of the adult mouse hippocampus. J Comp Neurol 424, 397-408 (2000). (Pubitemid 30670441)