Selective conversion of fibroblasts into peripheral sensory neurons

Nature Neuroscience

Volumn 18, Issue 1, 2015, Pages 25-35

  Blanchard, Joel W ^a   Eade, Kevin T ^a   Szůcs, Attila ^b,c   Lo Sardo, Valentina ^a   Tsunemoto, Rachel K ^a,d   Williams, Daniel ^a   Sanna, Pietro Paolo ^a   Baldwin, Kristin K ^a,d  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCITONIN GENE RELATED PEPTIDE; CALCIUM; LIGAND; MESSENGER RNA; NEUROGENIN 1; NEUROGENIN 2; NEUROTROPHIN 3 RECEPTOR; PROTEIN TYROSINE KINASE A; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR POU4F1; TRANSIENT RECEPTOR POTENTIAL CHANNEL; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; NERVE PROTEIN; NEUROG1 PROTEIN, HUMAN; NEUROG1 PROTEIN, MOUSE; NEUROG2 PROTEIN, HUMAN; NEUROG2 PROTEIN, MOUSE; POU4F1 PROTEIN, HUMAN; POU4F1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL ASSAY; CELL METABOLISM; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO CELL; FIBROBLAST; HUMAN; HUMAN CELL; MEMBRANE STEADY POTENTIAL; MOUSE; NERVE FIBER; NEUROFILAMENT; NONHUMAN; PERIPHERAL SENSORY NEURON; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY NERVE CELL; SYNAPSE VESICLE; TENDON RECEPTOR; TRANSIENT EXPRESSION; ANIMAL; CYTOLOGY; FEMALE; GENETICS; PAIN RECEPTOR; PATCH CLAMP TECHNIQUE; PERIPHERAL NERVOUS SYSTEM; PHYSIOLOGY; PREGNANCY; ULTRASTRUCTURE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; FEMALE; FIBROBLASTS; HUMANS; MICE; NERVE TISSUE PROTEINS; NOCICEPTORS; PATCH-CLAMP TECHNIQUES; PERIPHERAL NERVOUS SYSTEM; PREGNANCY; RECEPTOR, TRKC; SENSORY RECEPTOR CELLS; TRANSCRIPTION FACTOR BRN-3A;

EID: 84925286143     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3887     Document Type: Article

References (46)

1. Finnerup, N.B., Sindrup, S.H. & Jensen, T.S. The evidence for pharmacological treatment of neuropathic pain. Pain 150, 573-581 (2010).
2. Scholz, J. & Woolf, C.J. Can we conquer pain? Nat. Neurosci. 5, 1062-1067 (2002).
3. Koeppen, A.H. et al. The dorsal root ganglion in Friedreich's ataxia. Acta Neuropathol. 118, 763-776 (2009).
4. Riera, C.E. et al. TRPV1 pain receptors regulate longevity and metabolism by neuropeptide signaling. Cell 157, 1023-1036 (2014).
5. Dib-Hajj, S.D., Yang, Y., Black, J.A. & Waxman, S.G. The Na(V)1.7 sodium channel: from molecule to man. Nat. Rev. Neurosci. 14, 49-62 (2013).
6. Marmigère, F. & Ernfors, P. Specifcation and connectivity of neuronal subtypes in the sensory lineage. Nat. Rev. Neurosci. 8, 114-127 (2007).
7. Patapoutian, A., Tate, S. & Woolf, C.J. Transient receptor potential channels: targeting pain at the source. Nat. Rev. Drug Discov. 8, 55-68 (2009).
8. Malmberg, A.B., Martin, W.J., Trafton, J. & Petersen-Zeitz, K.R. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288, 306-313 (2000).
9. Peier, A.M. et al. TRP channel that senses cold stimuli and menthol. Cell 108, 705-715 (2002).
10. McKemy, D.D., Neuhausser, W.M. & Julius, D. Identifcation of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416, 52-58 (2002).
11. Macpherson, L.J. et al. Noxious compounds activate TRPA1 ion channels through covalent modifcation of cysteines: Abstract: Nature. Nature 445, 541-545 (2007).
12. Han, L. et al. A subpopulation of nociceptors specifcally linked to itch. Nat. Neurosci. 16, 174-182 (2013).
13. Sikand, P., Dong, X. & LaMotte, R.H. BAM8-22 peptide produces itch and nociceptive sensations in humans independent of histamine release. J. Neurosci. 31, 7563-7567 (2011).
14. Liu, Q. et al. Sensory neuron-specifc GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell 139, 1353-1365 (2009).
15. Bell, J.K., McQueen, D.S. & Rees, J.L. Involvement of histamine H4 and H1 receptors in scratching induced by histamine receptor agonists in BalbC mice. Br. J. Pharmacol. 142, 374-380 (2004).
16. Rubin, L.L. Stem cells and drug discovery: the beginning of a new era? Cell 132, 549-552 (2008).
17. Lanier, L.H. Variability in the pain threshold. Science 97, 49-50 (1943).
18. Nielsen, C.S., Price, D.D., Vassend, O., Stubhaug, A. & Harris, J.R. Characterizing individual differences in heat-pain sensitivity. Pain 119, 65-74 (2005).
19. Paul, S.M. et al. How to improve R&D productivity: the pharmaceutical industry's grand challenge. Nat. Rev. Drug Discov. 9, 203-214 (2010).
20. Chambers, S.M. et al. Combined small-molecule inhibition accelerates developmental timing and converts human pluripotent stem cells into nociceptors. Nat. Biotechnol. 30, 715-720 (2012).
21. Caiazzo, M. et al. Direct generation of functional dopaminergic neurons from mouse and human fbroblasts. Nature 476, 224-227 (2011).
22. Son, E.Y. et al. Conversion of mouse and human fbroblasts into functional spinal motor neurons. Cell Stem Cell 9, 205-218 (2011).
23. Liu, M.-L. et al. Small molecules enable neurogenin 2 to effciently convert human fbroblasts into cholinergic neurons. Nat. Commun. 4, 2183 (2013).
24. Pang, Z.P. et al. Induction of human neuronal cells by defned transcription factors. Nature 476, 220-223 (2011).
25. Pfsterer, U. et al. Direct conversion of human fbroblasts to dopaminergic neurons. Proc. Natl. Acad. Sci. USA 108, 10343-10348 (2011).
26. Vierbuchen, T. et al. Direct conversion of fbroblasts to functional neurons by defned factors. Nature 463, 1035-1041 (2010).
27. Kim, J. et al. Functional integration of dopaminergic neurons directly converted from mouse fbroblasts. Cell Stem Cell 9, 413-419 (2011).
28. Chanda, S. et al. Generation of induced neuronal cells by the single reprogramming factor ASCL1. Stem Cell Reports 3, 282-296 (2014).
29. Ma, Q., Fode, C., Guillemot, F. & Anderson, D.J. Neurogenin1 and neurogenin2 control two distinct waves of neurogenesis in developing dorsal root ganglia. Genes Dev. 13, 1717-1728 (1999).
30. Lanier, J., Dykes, I.M., Nissen, S., Eng, S.R. & Turner, E.E. Brn3a regulates the transition from neurogenesis to terminal differentiation and represses non-neural gene expression in the trigeminal ganglion. Dev. Dyn. 238, 3065-3079 (2009).
31. Ma, Q., Chen, Z., Barrantes, I.D.B., Luis de la Pompa, J. & Anderson, D.J. Neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20, 469-482 (1998).
32. McEvilly, R.J. et al. Requirement for Brn-3.0 in differentiation and survival of sensory and motor neurons. Nature 384, 574-577 (1996).
33. Boland, M.J. et al. Adult mice generated from induced pluripotent stem cells. Nature 461, 91-94 (2009).
34. Ferri, G.L. et al. Neuronal intermediate flaments in rat dorsal root ganglia: differential distribution of peripherin and neuroflament protein immunoreactivity and effect of capsaicin. Brain Res. 515, 331-335 (1990).
35. Fornaro, M. et al. Neuronal intermediate flament expression in rat dorsal root ganglia sensory neurons: an in vivo and in vitro study. Neuroscience 153, 1153-1163 (2008).
36. Lallemend, F. & Ernfors, P. Molecular interactions underlying the specifcation of sensory neurons. Trends Neurosci. 35, 373-381 (2012).
37. Landry, M., Bouali-Benazzouz, R., Mestikawy El, S., Ravassard, P. & Nagy, F.D.R. Expression of vesicular glutamate transporters in rat lumbar spinal cord, with a note on dorsal root ganglia. J. Comp. Neurol. 468, 380-394 (2004).
38. Li, L. et al. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147, 1615-1627 (2011).
39. Dykes, I.M., Lanier, J., Eng, S.R. & Turner, E.E. Brn3a regulates neuronal subtype specifcation in the trigeminal ganglion by promoting Runx expression during sensory differentiation. Neural Dev. 5, 3 (2010).
40. Sun, Y. et al. A central role for Islet1 in sensory neuron development linking sensory and spinal gene regulatory programs. Nat. Neurosci. 11, 1283-1293 (2008).
41. Fariñas, I. et al. Characterization of neurotrophin and Trk receptor functions in developing sensory ganglia: direct NT-3 activation of TrkB neurons in vivo. Neuron 21, 325-334 (1998).
42. Moqrich, A. et al. Expressing TrkC from the TrkA locus causes a subset of dorsal root ganglia neurons to switch fate. Nat. Neurosci. 7, 812-818 (2004).
43. Barrett, G.L. & Bartlett, P. F. The p75 nerve growth factor receptor mediates survival or death depending on the stage of sensory neuron development. Proc. Natl. Acad. Sci. USA 91, 6501-6505 (1994).
44. McMahon, S.B., Armanini, M.P., Ling, L.H. & Phillips, H.S. Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identifed peripheral targets. Neuron 12, 1161-1171 (1994).
45. Losick, R. & Desplan, C. Stochasticity and cell fate. Science 320, 65-68 (2008).
46. Addis, R.C. et al. Effcient conversion of astrocytes to functional midbrain dopaminergic neurons using a single polycistronic vector. PLoS ONE 6, e28719 (2011).