Enhanced neurogenesis in the hippocampal dentate gyrus during antigen-induced arthritis in adult rat - A crucial role of immunization

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Leuchtweis, Johannes ^a   Boettger, Michael K ^a,b   Niv, Fanny ^a   Redecker, Christoph ^a   Schaible, Hans Georg ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b BAYER PHARMA AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; BROXURIDINE; FREUND ADJUVANT;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN INDUCED ARTHRITIS; ARTHRITIS; ARTICLE; CELL COUNT; CONTROLLED STUDY; DENTATE GYRUS; DISEASE ASSOCIATION; FEMALE; HIPPOCAMPUS; HYPERALGESIA; IMMUNIZATION; INFLAMMATION; KNEE PAIN; KNEE SWELLING; LOCOMOTION; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGIC DISEASE; NOCICEPTION; NONHUMAN; RANGE OF MOTION; RAT; ANIMAL; CYTOLOGY; EXPERIMENTAL ARTHRITIS; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ARTHRITIS, EXPERIMENTAL; DENTATE GYRUS; FEMALE; IMMUNIZATION; INFLAMMATION; NEUROGENESIS; NEURONS; RATS;

EID: 84896755782     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089258     Document Type: Article

References (60)

1. Lampa J, Westman M, Kadetoff D, Nordenstedt Agréus A, Le Maitre E, et al. (2012) Peripheral inflammatory disease associated with centrally activated IL-1 system in humans and mice. Proc Natl Acad Sci U S A 109: 12728-12733.
2. Phillips K, Clauw DJ (2013) Central pain mechanisms in the rheumatic diseases. Arthritis Rheum 65: 291-302.
3. Schaible H-G, Ebersberger A, Natura G (2011) Update on peripheral mechanisms of pain: beyond prostaglandins and cytokines. Arthritis Res Ther 13: 210.
4. Schaible H-G, Richter F, Ebersberger A, Boettger MK, Vanegas H, et al. (2009) Joint pain. Exp Brain Res 196: 153-162.
5. McMahon SB, Malcangio M (2009) Current challenges in glia-pain biology. Neuron 64: 46-54.
6. Bushnell MC, Ceko M, Low LA (2013) Cognitive and emotional control of pain and its disruption in chronic pain. Nature Rev Neurosci 14: 502-511.
7. Straub RH, Cutolo M (2001) Involvement of the hypothalamic-pituitary- adrenal/gonadal axis and the peripheral nervous system in rheumatoid arthritis. Arthritis Rheum 44: 493-507. (Pubitemid 32234605)
8. Gage FH (2002) Neurogenesis in the adult brain. J Neurosci 22: 612-613.
9. Gross CG (2000) Neurogenesis in the adult brain: death of a dogma. Nature Rev Neurosci 1: 67-73.
10. Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197: 1092-1094. (Pubitemid 8170019)
11. Lledo P-M, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nature Rev Neurosci 7: 179-193. (Pubitemid 43292464)
12. Bruel-Jungerman E, Rampon C, Laroche S (2007) Adult hippocampal neurogenesis, synaptic plasticity and memory: facts and hypotheses. Reviews Neurosci 18: 93-114.
13. Deng W, Aimone JB, Gage FH (2010) New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nature Rev Neurosci 11: 339-350.
14. Inokuchi K (2011) Adult neurogenesis and modulation of neural circuit function. Curr Opin Neurobiol 21: 360-364.
15. van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neurosci 2: 266-270. (Pubitemid 30491298)
16. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27: 447-452. (Pubitemid 38951037)
17. Kuhn H, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16: 2027-2033. (Pubitemid 26144015)
18. Czéh B, Welt T, Fischer AK, Erhardt A, Schmitt W, et al. (2002) Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biological Psychiat 52: 1057-1065. (Pubitemid 35379963)
19. Gould E, McEwen BS, Tanapat P, Galea LAM, Fuchs E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17: 2492-2498. (Pubitemid 27137415)
20. Malberg JE, Duman RS (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsycho-pharmacol 28: 1562-1571. (Pubitemid 41070856)
21. Pham K, Nacher J, Hof PR, McEwen BS (2003) Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 17: 879-886. (Pubitemid 36315258)
22. Vollmayr B, Simonis C, Weber S, Gass P, Henn F (2003) Reduced cell proliferation in the dentate gyrusis not correlated with the development of learned helplessness. Biological Psychiatry 54: 1035-1040. (Pubitemid 37415038)
23. Madsen TM, Kristjansen PEG, Bolwig TG, Wörtwein G (2003) Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119: 635-642. (Pubitemid 36694791)
24. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386: 493-495. (Pubitemid 27164074)
25. Jessberger S, Nakashima K, Clemenson GD, Mejia E, Mathews E, et al. (2007a) Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci 27: 5967-5975. (Pubitemid 46849752)
26. Jessberger S, Zhao C, Toni N, Clemenson GD, Li Y, et al. (2007b) Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J Neurosci 27: 9400-9407. (Pubitemid 47358204)
27. Niv F, Keiner S, Krishna K, Witte OW, Lie DC, et al. (2012) Aberrant neurogenesis after stroke: A retroviral cell labeling study. Stroke 43: 2468-2475.
28. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, et al. (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17: 3727-3738. (Pubitemid 27200597)
29. Cacci E, Claasen J-H, Kokaia Z (2005) Microglia-derived tumor necrosis factor-α exaggerates death of newborn hippocampal progenitor cells in vitro. J Neurosci Res 80: 80789-80797.
30. Butovsky O, Ziv Y, Schwartz A, Landa G, Talpalar AE, et al. (2006) Microglia activated by IL-4 or IFN-γ differentially induce neurogenesis and oligoden-drogenesis from adult stem/progenitor cells. Mol Cell Neurosci 31: 149-160. (Pubitemid 43049908)
31. Ekdahl CT, Claasen J-H, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc National Acad Sci USA 100: 13632-13637. (Pubitemid 37444791)
32. Monje ML, Toda H, Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765. (Pubitemid 37505739)
33. Wu C-W, Chen Y-C, Yu L, Chen H-I, Jen CJ, et al. (2007) Treadmill exercise counteracts the suppressive effects of peripheral lipopolysaccharide on hippocampal neurogenesis and learning and memory. J Neurochem 103: 2471-2481. (Pubitemid 350173589)
34. Wolf SA, Steiner B, Wengner A, Lipp M, Kammertoens T, et al. (2009) Kempermann G. Adaptive peripheral immune response increases proliferation of neural precursor cells in the adult hippocampus. FASEB J 23: 3121-3128.
35. Boettger MK, Hensellek S, Richter F, Gajda M, Stöckigt R, et al. (2008) Antinociceptive effects of tumor necrosis factor alpha neutralization in a rat model of antigen-induced arthritis: evidence of a neuronal target. Arthritis Rheum 58: 2368-2378.
36. Boettger MK, Leuchtweis J, Schaible H-G, Schmidt M (2011) Videoradio-graphic analysis of the range of motion in unilateral experimental knee joint arthritis in rats. Arthritis Res Ther 13: R79.
37. Webster JI, Tonelli L, Sternberg EM (2002) Neuroendocrine regulation of immunity. Annu Rev Immunol 20: 125-163. (Pubitemid 34295785)
38. Griffiths RJ (1992) Characterisation and pharmacological sensitivity of antigen arthritis induced by methylated bovine serum albumin in the rat. Agents Actions 35: 88-95.
39. Leuchtweis J, Imhof AK, Montechiaro F, Schaible H-G, Boettger MK (2010) Validation of the digital pressure application measurement (PAM) device for detection of primary mechanical hyperalgesia in rat and mouse antigen-induced knee joint arthritis. Meth Findings Exp Clin Pharmacol 32: 575-583.
40. Boettger MK, Leuchtweis J, Kümmel D, Gajda M, Bräuer R, et al. (2010) Differential effects of locally and systemically administered soluble glycoprotein 130 on pain and inflammation in experimental arthritis. Arthritis Res Ther 12: R140.
41. Kluska MM, Witte OW, Bolz J, Redecker C (2005) Neurogenesis in the adult dentate gyrus after cortical infarcts: Effects of infarct location, N-methyl-d-aspartate receptor blockade and anti-inflammatory treatment. Neuroscience 135: 723-725.
42. Urbach A, Redecker C, Witte OW (2008) Induction of neurogenesis in the adult dentate gyrus by cortical spreading depression. Stroke 39: 3064-3072.
43. Wurm F, Keiner S, Kunze A, Witte OW, Redecker C (2007) Effects of skilled forelimb training on hippocampal neurogenesis and spatial learning after focal cortical infarcts in the adult rat brain. Stroke 38: 2833-2840. (Pubitemid 47494025)
44. Bellinzona M, Gobbel GT, Shinohara C, Fike JR (1996) Apoptosis is induced in the subependyma of young adult rats by ionizing irradiation. Neurosci Lett 208: 163-166. (Pubitemid 26141526)
45. Parent JM, Tada E, Fike JR, Lowenstein DH (1999) Inhibition of dentate granule cell neurogenesis with brain irradiation does not prevent seizure-induced mossy fiber synaptic reorganization in the rat. J Neurosci 19: 4508-4519. (Pubitemid 29241101)
46. Peißner W, Kocher M, Treuer H, Gillardon F (1999) Ionizing radiation-induced apoptosis of proliferating stem cells in the dentate gyrus of the adult rat hippocampus. Mol Brain Res 71: 61-68. (Pubitemid 29320056)
47. Shinohara C, Gobbel GT, Lamborn KR, Tada E, Fike JR (1997) Apoptosis in the subependyma of young adult rats after single and fractionated doses of Xrays. Cancer Research 57: 2694-2702. (Pubitemid 27283782)
48. Tada E, Parent JM, Lowenstein DH, Fike JR (2000) X-irradiation causes a prolonged reduction in cell proliferation in the dentate gyrus of adult rats. Neuroscience 99: 33-41. (Pubitemid 30495550)
49. Mizumatsu S, Monje ML, Morhardt DR, Rola R, Palmer TD, et al. (2003) Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res 63: 4021-4027. (Pubitemid 36917922)
50. Arvidsson A, Kokaia Z, Lindvall O (2001) N-methyl-d-aspartate receptor-mediated increase of neurogenesis in adult rat dentate gyrus following stroke. Eur J Neurosci 14: 10-18. (Pubitemid 32738469)
51. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, et al. (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17: 2042-2046. (Pubitemid 36713965)
52. Droste SK, Gesing A, Ulbricht S, Müller MB, Linthorst ACE, et al. (2003) Effects of long-term voluntary exercise on the mouse hypothalamic- pituitary-adrenocortical axis. Endocrinol 144: 3012-3023. (Pubitemid 36819903)
53. Ekstrand J, Hellsten J, Tingström A (2008) Environmental enrichment, exercise and corticosterone affect endothelial cell proliferation in adult rat hippocampus and prefrontal cortex. Neurosci Lett 442: 203-207.
54. van Praag H (2008) Neurogenesis and exercise: Past and future directions. Neuromol Med 10: 128-140.
55. Duric V, McCarson KE (2006) Persistent pain produces stress-like alterations in hippocampal neurogenesis and gene expression. J Pain 7: 544-555. (Pubitemid 44119288)
56. Kaneko N, Kudo K, Mabuchi T, Takemoto K, Fujimaki K, et al. (2006) Suppression of cell proliferation by interferon-alpha through interleukin-1 production in adult rat dentate gyrus. Neuropsychopharmacol 31: 2619-2626. (Pubitemid 44764159)
57. Vallières L, Campbell IL, Gage FH, Sawchenko PE (2002) Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6. J Neurosci 22: 486-492. (Pubitemid 34049087)
58. Wong EYH, Herbert J (2004) The corticoid environment: a determining factor for neural progenitors' survival in the adult hippocampus. Eur J Neurosci 20: 2491-2498. (Pubitemid 39573766)
59. Baron R, Nemirovsky A, Harpaz I, Cohen H, Owens T, et al. (2008) IFN-γ enhances neurogenesis in wild-type mice and in a mouse model of Alzheimer's disease. FASEB J 22: 2843-2852.
60. Schurigt U, Stopfel N, Huckel M, Pfirschke C, Wiederanders B, et al. (2005) Local expression of matrix metalloproteinases, cathepsins, and their inhibitors during the development of murine antigen-induced arthritis. Arthritis Res Ther 7: R174.