PACAP deficiency sensitizes nigrostriatal dopaminergic neurons to paraquat-induced damage and modulates central and peripheral inflammatory activation in mice

Neuroscience

Volumn 240, Issue , 2013, Pages 277-286

  Watson, M B ^a   Nobuta, H ^b   Abad, C ^a   Lee, S K ^a   Bala, N ^a   Zhu, C ^a   Richter, F ^a   Chesselet, M F ^a,b   Waschek, J A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Microglia; PACAP; Paraquat; Parkinson's disease; Pesticide; Tyrosine hydroxylase

Indexed keywords

HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; NEUROPEPTIDE; PARAQUAT; TUMOR NECROSIS FACTOR ALPHA; TYROSINE 3 MONOOXYGENASE; VESICULAR MONOAMINE TRANSPORTER 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; GENE EXPRESSION; HEREDITY; IMMUNOCOMPETENT CELL; KNOCKOUT MOUSE; MALE; MICROGLIA; MITOCHONDRION; MOUSE; NERVE CELL LESION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RISK FACTOR; SUBSTANTIA NIGRA; TH1 CELL; TH17 CELL; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; CALCIUM-BINDING PROTEINS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; DOPAMINERGIC NEURONS; HERBICIDES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MICROGLIA; NEUROTOXICITY SYNDROMES; PARAQUAT; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; SUBSTANTIA NIGRA; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA; TYROSINE 3-MONOOXYGENASE;

EID: 84876299964     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.03.002     Document Type: Article

References (62)

1. Armstrong B.D., Abad C., Chhith S., Cheung-Lau G., Hajji O.E., Nobuta H., Waschek J.A. Impaired nerve regeneration and enhanced neuroinflammatory response in mice lacking pituitary adenylyl cyclase activating peptide. Neuroscience 2008, 151:63-73.
2. Baba Y., Kuroiwa A., Uitti R.J., Wszolek Z.K., Yamada T. Alterations of T-lymphocyte populations in Parkinson disease. Parkinsonism Relat Disord 2005, 11:493-498.
3. Baldi I., Cantagrel A., Lebailly P., Tison F., Dubroca B., Chrysostome V., Dartigues J.F., Brochard P. Association between Parkinson's disease and exposure to pesticides in southwestern France. Neuroepidemiology 2003, 22:305-310.
4. Beaudet M.M., Braas K.M., May V. Pituitary adenylate cyclase activating polypeptide (PACAP) expression in sympathetic preganglionic projection neurons to the superior cervical ganglion. J Neurobiol 1998, 36:325-336.
5. Bobrovskaya L., Gelain D.P., Gilligan C., Dickson P.W., Dunkley P.R. PACAP stimulates the sustained phosphorylation of tyrosine hydroxylase at serine 40. Cell Signal 2007, 19:1141-1149.
6. Bower J.H., Maraganore D.M., Peterson B.J., Ahlskog J.E., Rocca W.A. Immunologic diseases, anti-inflammatory drugs, and Parkinson disease: a case-control study. Neurology 2006, 67:494-496.
7. Brochard V., Combadiere B., Prigent A., Laouar Y., Perrin A., Beray-Berthat V., Bonduelle O., Alvarez-Fischer D., Callebert J., Launay J.M., et al. Infiltration of CD4+ lymphocytes into the brain contributes to neurodegeneration in a mouse model of Parkinson disease. J Clin Invest 2009, 119:182-192.
8. Brooks A.I., Chadwick C.A., Gelbard H.A., Cory-Slechta D.A., Federoff H.J. Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss. Brain Res 1999, 823:1-10.
9. Chen H., Jacobs E., Schwarzschild M.A., McCullough M.L., Calle E.E., Thun M.J., Ascherio A. Nonsteroidal antiinflammatory drug use and the risk for Parkinson's disease. Ann Neurol 2005, 58:963-967.
10. Chung C.Y., Seo H., Sonntag K.C., Brooks A., Lin L., Isacson O. Cell type-specific gene expression of midbrain dopaminergic neurons reveals molecules involved in their vulnerability and protection. Hum Mol Genet 2005, 14:1709-1725.
11. Colwell C.S., Michel S., Itri J., Rodriguez W., Tam J., Lelievre V., Hu Z., Waschek J.A. Selective deficits in the circadian light response in mice lacking PACAP. Am J Physiol Regul Integr Comp Physiol 2004, 287:R1194-R1201.
12. Corbitt J., Vivekananda J., Wang S.S., Strong R. Transcriptional and posttranscriptional control of tyrosine hydroxylase gene expression during persistent stimulation of pituitary adenylate cyclase-activating polypeptide receptors on PC12 cells: regulation by protein kinase A-dependent and protein kinase A-independent pathways. J Neurochem 1998, 71:478-486.
13. Costello S., Cockburn M., Bronstein J., Zhang X., Ritz B. Parkinson's disease and residential exposure to maneb and paraquat from agricultural applications in the central valley of California. Am J Epidemiol 2009, 169:919-926.
14. Delgado M., Leceta J., Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit the production of inflammatory mediators by activated microglia. J Leukoc Biol 2003, 73:155-164.
15. Efron B., Tibshirani R. Statistical data analysis in the computer age. Science 1991, 253:390-395.
16. Engel L.S., Checkoway H., Keifer M.C., Seixas N.S., Longstreth W.T., Scott K.C., Hudnell K., Anger W.K., Camicioli R. Parkinsonism and occupational exposure to pesticides. Occup Environ Med 2001, 58:582-589.
17. Fernagut P.O., Hutson C.B., Fleming S.M., Tetreaut N.A., Salcedo J., Masliah E., Chesselet M.F. Behavioral and histopathological consequences of paraquat intoxication in mice: effects of alpha-synuclein over-expression. Synapse 2007, 61:991-1001.
18. Fitzmaurice A.G., Rhodes S.L., Lulla A., Murphy N.P., Lam H.A., O'Donnell K.C., Barnhill L., Casida J.E., Cockburn M., Sagasti A., Stahl M.C., Maidment N.T., Ritz B., Bronstein J.M. Aldehyde dehydrogenase inhibition as a pathogenic mechanism in Parkinson disease. Proc Natl Acad Sci U S A 2013, 110:636-641.
19. Forno L.S., DeLanney L.E., Irwin I., Di Monte D., Langston J.W. Astrocytes and Parkinson's disease. Prog Brain Res 1992, 94:429-436.
20. Gerhard A., Pavese N., Hotton G., Turkheimer F., Es M., Hammers A., Eggert K., Oertel W., Banati R.B., Brooks D.J. In vivo imaging of microglial activation with [11C](R)-PK11195 PET in idiopathic Parkinson's disease. Neurobiol Dis 2006, 21:404-412.
21. Ghatei M.A., Takahashi K., Suzuki Y., Gardiner J., Jones P.M., Bloom S.R. Distribution, molecular characterization of pituitary adenylate cyclase-activating polypeptide and its precursor encoding messenger RNA in human and rat tissues. J Endocrinol 1993, 136:159-166.
22. Gorell J.M., Peterson E.L., Rybicki B.A., Johnson C.C. Multiple risk factors for Parkinson's disease. J Neurol Sci 2004, 217:169-174.
23. Guillot T.S., Richardson J.R., Wang M.Z., Li Y.J., Taylor T.N., Ciliax B.J., Zachrisson O., Mercer A., Miller G.W. PACAP38 increases vesicular monoamine transporter 2 (VMAT2) expression and attenuates methamphetamine toxicity. Neuropeptides 2008, 42:423-434.
24. Hamza T.H., Chen H., Hill-Burns E.M., Rhodes S.L., Montimurro J., Kay D.M., Tenesa A., Kusel V.I., Sheehan P., Eaaswarkhanth M., et al. Genome-wide gene-environment study identifies glutamate receptor gene GRIN2A as a Parkinson's disease modifier gene via interaction with coffee. PLoS Genet 2012, 7:e1002237.
25. Hirsch E.C. Glial cells and Parkinson's disease. J Neurol 2000, 247(Suppl. 2):II58-II62.
26. Houchi H., Azuma M., Kitamura K., Okuno M., Oka M. Pituitary adenylate cyclase-activating polypeptide stimulates the synthesis of dopamine in cultured bovine adrenal chromaffin cells. Hypertens Res 1995, 18(Suppl. 1):S169-S171.
27. Kambe Y., Miyata A. Role of Mitochondrial Activation in PACAP Dependent Neurite Outgrowth. J Mol Neurosci 2012, 48:550-557.
28. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996, 19:312-318.
29. Manthripragada A.D., Schernhammer E.S., Qiu J., Friis S., Wermuth L., Olsen J.H., Ritz B. Non-steroidal anti-inflammatory drug use and the risk of Parkinson's disease. Neuroepidemiology 2011, 36:155-161.
30. McCormack A.L., Thiruchelvam M., Manning-Bog A.B., Thiffault C., Langston J.W., Cory-Slechta D.A., Di Monte D.A. Environmental risk factors and Parkinson's disease: selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiol Dis 2002, 10:119-127.
31. McGeer P.L., Itagaki S., Boyes B.E., McGeer E.G. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 1988, 38:1285-1291.
32. Meurers B.H., Zhu C., Fernagut P.O., Richter F., Hsia Y.C., Fleming S.M., Oh M., Elashoff D., Dicarlo C.D., Seaman R.L., Chesselet M.F. Low dose rotenone treatment causes selective transcriptional activation of cell death related pathways in dopaminergic neurons in vivo. Neurobiol Dis 2009, 33:182-192.
33. Mogi M., Nagatsu T. Neurotrophins and cytokines in Parkinson's disease. Adv Neurol 1999, 80:135-139.
34. Mogi M., Harada M., Kondo T., Riederer P., Inagaki H., Minami M., Nagatsu T. Interleukin-1 beta, interleukin-6, epidermal growth factor and transforming growth factor-alpha are elevated in the brain from parkinsonian patients. Neurosci Lett 1994, 180:147-150.
35. Moser A., Scholz J., Gansle A. Pituitary adenylate cyclase-activating polypeptide (PACAP-27) enhances tyrosine hydroxylase activity in the nucleus accumbens of the rat. Neuropeptides 1999, 33:492-497.
36. Nagatsu T., Mogi M., Ichinose H., Togari A. Changes in cytokines and neurotrophins in Parkinson's disease. J Neural Transm Suppl 2000, 60:277-290.
37. Nagatsu T., Mogi M., Ichinose H., Togari A. Cytokines in Parkinson's disease. J Neural Transm Suppl 2000, 58:143-151.
38. Ohtaki H., Nakamachi T., Dohi K., Aizawa Y., Takaki A., Hodoyama K., Yofu S., Hashimoto H., Shintani N., Baba A., et al. Pituitary adenylate cyclase-activating polypeptide (PACAP) decreases ischemic neuronal cell death in association with IL-6. Proc Natl Acad Sci U S A 2006, 103:7488-7493.
39. Ossowska K., Wardas J., Smialowska M., Kuter K., Lenda T., Wieronska J.M., Zieba B., Nowak P., Dabrowska J., Bortel A., et al. A slowly developing dysfunction of dopaminergic nigrostriatal neurons induced by long-term paraquat administration in rats: an animal model of preclinical stages of Parkinson's disease?. Eur J Neurosci 2005, 22:1294-1304.
40. Ouchi Y., Yagi S., Yokokura M., Sakamoto M. Neuroinflammation in the living brain of Parkinson's disease. Parkinsonism Relat Disord 2009, 15(Suppl. 3):S200-S204.
41. Peng J., Mao X.O., Stevenson F.F., Hsu M., Andersen J.K. The herbicide paraquat induces dopaminergic nigral apoptosis through sustained activation of the JNK pathway. J Biol Chem 2004, 279:32626-32632.
42. Purisai M.G., McCormack A.L., Cumine S., Li J., Isla M.Z., Di Monte D.A. Microglial activation as a priming event leading to paraquat-induced dopaminergic cell degeneration. Neurobiol Dis 2007, 25:392-400.
43. Rappold P.M., Lynd-Balta E., Joseph S.A. P2X7 receptor immunoreactive profile confined to resting and activated microglia in the epileptic brain. Brain Res 2006, 1089:171-178.
44. Reglodi D., Lubics A., Tamas A., Szalontay L., Lengvari I. Pituitary adenylate cyclase activating polypeptide protects dopaminergic neurons and improves behavioral deficits in a rat model of Parkinson's disease. Behav Brain Res 2004, 151:303-312.
45. Reglodi D., Tamas A., Lubics A., Szalontay L., Lengvari I. Morphological and functional effects of PACAP in 6-hydroxydopamine-induced lesion of the substantia nigra in rats. Regul Pept 2004, 123:85-94.
46. Reglodi D., Kiss P., Lubics A., Tamas A. Review on the protective effects of PACAP in models of neurodegenerative diseases in vitro and in vivo. Curr Pharm Des 2011, 17:962-972.
47. Reglodi D., Kiss P., Szabadfi K., Atlasz T., Gabriel R., Horvath G., Szakaly P., Sandor B., Lubics A., Laszlo E., Farkas J., Matkovits A., Brubel R., Hashimoto H., Ferencz A., Vincze A., Helyes Z., Welke L., Lakatos A., Tamas A. PACAP is an endogenous protective factor-insights from PACAP-deficient mice. J Mol Neurosci 2012, 48:482-492.
48. Reynolds A.D., Banerjee R., Liu J., Gendelman H.E., Mosley R.L. Neuroprotective activities of CD4+CD25+ regulatory T cells in an animal model of Parkinson's disease. J Leukoc Biol 2007, 82:1083-1094.
49. Ritz B.R., Manthripragada A.D., Costello S., Lincoln S.J., Farrer M.J., Cockburn M., Bronstein J. Dopamine transporter genetic variants and pesticides in Parkinson's disease. Environ Health Perspect 2009, 117:964-969.
50. Ritz B., Rhodes S.L., Bordelon Y., Bronstein J. Alpha-Synuclein genetic variants predict faster motor symptom progression in idiopathic Parkinson disease. PLoS One 2012, 7:e36199.
51. Stetler R.A., Gao Y., Zukin R.S., Vosler P.S., Zhang L., Zhang F., Cao G., Bennett M.V., Chen J. Apurinic/apyrimidinic endonuclease APE1 is required for PACAP-induced neuroprotection against global cerebral ischemia. Proc Natl Acad Sci U S A 2010, 107:3204-3209.
52. Streit W.J., Walter S.A., Pennell N.A. Reactive microgliosis. Prog Neurobiol 1999, 57:563-581.
53. Takei N., Skoglosa Y., Lindholm D. Neurotrophic and neuroprotective effects of pituitary adenylate cyclase-activating polypeptide (PACAP) on mesencephalic dopaminergic neurons. J Neurosci Res 1998, 54:698-706.
54. Tan Y.V., Abad C., Lopez R., Dong H., Liu S., Lee A., Gomariz R.P., Leceta J., Waschek J.A. Pituitary adenylyl cyclase-activating polypeptide is an intrinsic regulator of Treg abundance and protects against experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 2009, 106:2012-2017.
55. Tanner C.M., Kamel F., Ross G.W., Hoppin J.A., Goldman S.M., Korell M., Marras C., Bhudhikanok G.S., Kasten M., Chade A.R., et al. Rotenone, paraquat, and Parkinson's disease. Environ Health Perspect 2011, 119:866-872.
56. Ton T.G., Heckbert S.R., Longstreth W.T., Rossing M.A., Kukull W.A., Franklin G.M., Swanson P.D., Smith-Weller T., Checkoway H. Nonsteroidal anti-inflammatory drugs and risk of Parkinson's disease. Mov Disord 2006, 21:964-969.
57. Wahner A.D., Sinsheimer J.S., Bronstein J.M., Ritz B. Inflammatory cytokine gene polymorphisms and increased risk of Parkinson disease. Arch Neurol 2007, 64:836-840.
58. Wang G., Pan J., Tan Y.Y., Sun X.K., Zhang Y.F., Zhou H.Y., Ren R.J., Wang X.J., Chen S.D. Neuroprotective effects of PACAP27 in mice model of Parkinson's disease involved in the modulation of K(ATP) subunits and D2 receptors in the striatum. Neuropeptides 2008, 42:267-276.
59. Wang A., Costello S., Cockburn M., Zhang X., Bronstein J., Ritz B. Parkinson's disease risk from ambient exposure to pesticides. Eur J Epidemiol 2011, 26:547-555.
60. Watson M.B., Richter F., Lee S.K., Gabby L., Wu J., Masliah E., Effros R.B., Chesselet M.F. Regionally-specific microglial activation in young mice over-expressing human wildtype alpha-synuclein. Exp Neurol 2012, 237:318-334.
61. West M.J., Slomianka L., Gundersen H.J. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991, 231:482-497.
62. Yang S., Yang J., Yang Z., Chen P., Fraser A., Zhang W., Pang H., Gao X., Wilson B., Hong J.S., Block M.L. Pituitary adenylate cyclase-activating polypeptide (PACAP) 38 and PACAP4-6 are neuroprotective through inhibition of NADPH oxidase: potent regulators of microglia-mediated oxidative stress. J Pharmacol Exp Ther 2006, 319:595-603.