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Translational Neurodegeneration

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Open Access 01-12-2012 | Research

Directed migration of human neural progenitor cells to interleukin-1β is promoted by chemokines stromal cell-derived factor-1 and monocyte chemotactic factor-1 in mouse brains

Authors: Yumei Wu, Qiang Chen, Hui Peng, Huanyu Dou, You Zhou, Yunlong Huang, Jialin C Zheng

Published in: Translational Neurodegeneration | Issue 1/2012

Abstract

Background

Neurogenesis, including the proliferation, migration and differentiation of neural progenitor cells (NPCs), is impaired in HIV-1 associated dementia (HAD). We previously demonstrated HIV-1-infected macrophages (HIV-MDM) regulate stromal cell-derived factor 1 (SDF-1) production in astrocytes through Interleukin-1β (IL-1β). Chemokines are known to induce NPC migration; however, it remains unclear how chemokines produced in inflammation regulate NPC migration.

Methods

The secretion of SDF-1 and Monocyte chemotactic preotein-1 (MCP-1) in astrocytes upon IL-1β stimulation was measured by ELISA assay. Human NPCs were injected parallel along with IL-1β, SDF-1 or MCP-1 intracranially into basal ganglion 1 mm apart in SCID mice, and immunofluorescent staining was used to study the survival and migration of injected human NPCs.

Results

SDF-1 and MCP-1 are secreted by astrocytes upon IL-1β stimulation in a time-dependent manner. Injected human NPCs survived in SCID mice and migrated towards sites of IL-1β, SDF-1 and MCP-1 injection.

Conclusions

In conclusion, chemokines SDF-1 or MCP-1 secreted by astrocytes in the presence of IL-1β injection are attractive to NPCs injected into SCID mouse brains, suggesting that SDF-1 and MCP-1 play important roles in NPC migration during neuroinflammation.

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Okamoto S, Kang YJ, Brechtel CW, Siviglia E, Russo R, Clemente A, Harrop A, McKercher S, Kaul M, Lipton SA: HIV/gp120 decreases adult neural progenitor cell proliferation via checkpoint kinase-mediated cell-cycle withdrawal and G1 arrest. Cell Stem Cell 2007, 1: 230-236. 10.1016/j.stem.2007.07.010CrossRefPubMed

Avgeropoulos NG, Burris GW, Ohlandt GW, Wesselingh SL, Markham RB, Tyor WR: Potential relationships between the presence of HIV, macrophages, and astrogliosis in SCID mice with HIV encephalitis. J NeuroAIDS 1998, 2: 1-20.PubMed

Langford D, Sanders VJ, Mallory M, Kaul M, Masliah E: Expression of stromal cell-derived factor 1alpha protein in HIV encephalitis. J Neuroimmunol 2002, 127: 115-126. 10.1016/S0165-5728(02)00068-1CrossRefPubMed

Rostasy K, Egles C, Chauhan A, Kneissl M, Bahrani P, Yiannoutsos C, Hunter DD, Nath A, Hedreen JC, Navia BA: SDF-1alpha is expressed in astrocytes and neurons in the AIDS dementia complex: an in vivo and in vitro study. J Neuropathol Exp Neurol 2003, 62: 617-626.PubMed

Cinque P, Vago L, Mengozzi M, Torri V, Ceresa D, Vicenzi E, Transidico P, Vagani A, Sozzani S, Mantovani A, et al.: Elevated cerebrospinal fluid levels of monocyte chemotactic protein-1 correlate with HIV-1 encephalitis and local viral replication. AIDS 1998, 12: 1327-1332. 10.1097/00002030-199811000-00014CrossRefPubMed

Conant K, Garzino-Demo A, Nath A, McArthur JC, Halliday W, Power C, Gallo RC, Major EO: Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation in AIDS dementia. Proc Natl Acad Sci USA 1998, 95: 3117-3121. 10.1073/pnas.95.6.3117PubMedCentralCrossRefPubMed

Lu M, Grove EA, Miller RJ: Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor. Proc Natl Acad Sci U S A 2002, 99: 7090-7095. 10.1073/pnas.092013799PubMedCentralCrossRefPubMed

Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR: Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998, 393: 595-599. 10.1038/31269CrossRefPubMed

Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, Bronson RT, Springer TA: Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci U S A 1998, 95: 9448-9453. 10.1073/pnas.95.16.9448PubMedCentralCrossRefPubMed

10.

Peng H, Huang Y, Rose J, Erichsen D, Herek S, Fujii N, Tamamura H, Zheng J: Stromal cell-derived factor 1-mediated CXCR4 signaling in rat and human cortical neural progenitor cells. J Neurosci Res 2004, 76: 35-50. 10.1002/jnr.20045CrossRefPubMed

11.

Belmadani A, Tran PB, Ren D, Assimacopoulos S, Grove EA, Miller RJ: The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. The Journal of neuroscience: the official journal of the Society for Neuroscience 2005, 25: 3995-4003. 10.1523/JNEUROSCI.4631-04.2005CrossRef

12.

Peng H, Erdmann N, Whitney N, Dou H, Gorantla S, Gendelman HE, Ghorpade A, Zheng J: HIV-1-infected and/or immune activated macrophages regulate astrocyte SDF-1 production through IL-1beta. Glia 2006, 54: 619-629. 10.1002/glia.20409PubMedCentralCrossRefPubMed

13.

Robin AM, Zhang ZG, Wang L, Zhang RL, Katakowski M, Zhang L, Wang Y, Zhang C, Chopp M: Stromal cell-derived factor 1alpha mediates neural progenitor cell motility after focal cerebral ischemia. Journal of cerebral blood flow and metabolism: official journal of the International Society of Cerebral Blood Flow and Metabolism 2006, 26: 125-134.CrossRef

14.

Xu Q, Wang S, Jiang X, Zhao Y, Gao M, Zhang Y, Wang X, Tano K, Kanehara M, Zhang W, Ishida T: Hypoxia-induced astrocytes promote the migration of neural progenitor cells via vascular endothelial factor, stem cell factor, stromal-derived factor-1alpha and monocyte chemoattractant protein-1 upregulation in vitro. Clin Exp Pharmacol Physiol 2007, 34: 624-631. 10.1111/j.1440-1681.2007.04619.xCrossRefPubMed

15.

van der Meer P, Ulrich AM, Gonzalez-Scarano F, Lavi E: Immunohistochemical analysis of CCR2, CCR3, CCR5, and CXCR4 in the human brain: potential mechanisms for HIV dementia. Exp Mol Pathol 2000, 69: 192-201. 10.1006/exmp.2000.2336CrossRefPubMed

16.

Coughlan CM, McManus CM, Sharron M, Gao Z, Murphy D, Jaffer S, Choe W, Chen W, Hesselgesser J, Gaylord H, et al.: Expression of multiple functional chemokine receptors and monocyte chemoattractant protein-1 in human neurons. Neuroscience 2000, 97: 591-600. 10.1016/S0306-4522(00)00024-5CrossRefPubMed

17.

Babcock AA, Kuziel WA, Rivest S, Owens T: Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J Neurosci 2003, 23: 7922-7930.PubMed

18.

Widera D, Holtkamp W, Entschladen F, Niggemann B, Zanker K, Kaltschmidt B, Kaltschmidt C: MCP-1 induces migration of adult neural stem cells. Eur J Cell Biol 2004, 83: 381-387. 10.1078/0171-9335-00403CrossRefPubMed

19.

Yan YP, Sailor KA, Lang BT, Park SW, Vemuganti R, Dempsey RJ: Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia. J Cereb Blood Flow Metab 2007, 27: 1213-1224. 10.1038/sj.jcbfm.9600432CrossRefPubMed

20.

Abrous DN, Koehl M, Le Moal M: Adult neurogenesis: from precursors to network and physiology. Physiol Rev 2005, 85: 523-569. 10.1152/physrev.00055.2003CrossRefPubMed

21.

Lie DC, Dziewczapolski G, Willhoite AR, Kaspar BK, Shults CW, Gage FH: The adult substantia nigra contains progenitor cells with neurogenic potential. J Neurosci 2002, 22: 6639-6649.PubMed

22.

Parent JM: Injury-induced neurogenesis in the adult mammalian brain. Neuroscientist 2003, 9: 261-272. 10.1177/1073858403252680CrossRefPubMed

23.

Guillemin GJ, Croitoru-Lamoury J, Dormont D, Armati PJ, Brew BJ: Quinolinic acid upregulates chemokine production and chemokine receptor expression in astrocytes. Glia 2003, 41: 371-381. 10.1002/glia.10175CrossRefPubMed

24.

Losy J, Zaremba J: Monocyte chemoattractant protein-1 is increased in the cerebrospinal fluid of patients with ischemic stroke. Stroke 2001, 32: 2695-2696. 10.1161/hs1101.097380CrossRefPubMed

25.

Fricker RA, Carpenter MK, Winkler C, Greco C, Gates MA, Bjorklund A: Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J Neurosci 1999, 19: 5990-6005.PubMed

26.

Magge SN, Malik SZ, Royo NC, Chen HI, Yu L, Snyder EY, O’Rourke DM, Watson DJ: Role of monocyte chemoattractant protein-1 (MCP-1/CCL2) in migration of neural progenitor cells toward glial tumors. J Neurosci Res 2009, 87: 1547-1555. 10.1002/jnr.21983CrossRefPubMed

27.

Gage FH: Mammalian neural stem cells. Science 2000, 287: 1433-1438. 10.1126/science.287.5457.1433CrossRefPubMed

28.

Horner PJ, Gage FH: Regenerating the damaged central nervous system. Nature 2000, 407: 963-970. 10.1038/35039559CrossRefPubMed

29.

Emsley JG, Mitchell BD, Kempermann G, Macklis JD: Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 2005, 75: 321-341. 10.1016/j.pneurobio.2005.04.002CrossRefPubMed

30.

Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O: Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002, 8: 963-970. 10.1038/nm747CrossRefPubMed

31.

Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC: Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004, 10: 858-864. 10.1038/nm1075CrossRefPubMed

32.

Peng H, Sun L, Jia B, Lan X, Zhu B, Wu Y, Zheng J: HIV-1-infected and immune-activated macrophages induce astrocytic differentiation of human cortical neural progenitor cells via the STAT3 pathway. PLoS One 2011, 6: e19439. 10.1371/journal.pone.0019439PubMedCentralCrossRefPubMed

33.

Karpus WJ, Ransohoff RM: Chemokine regulation of experimental autoimmune encephalomyelitis: Temporal and spatial expression patterns govern disease pathogenesis. J Immunol 1998, 161: 2667-2671.PubMed

34.

Johnstone M, Gearing AJ, Miller KM: A central role for astrocytes in the inflammatory response to beta- amyloid; chemokines, cytokines and reactive oxygen species are produced. J Neuroimmunol 1999, 93: 182-193. 10.1016/S0165-5728(98)00226-4CrossRefPubMed

35.

Minami M, Satoh M: Chemokines as mediators for intercellular communication in the brain. Nippon Yakurigaku Zasshi 2000, 115: 193-200. 10.1254/fpj.115.193CrossRefPubMed

36.

Drew TKPD: Cytokines and Brain. In Inflammatory disorders of the nervous system: pathogenesis, immunology, and clinical management. Volume 1. Edited by: Alireza Minagar JSA. Humana Press, Totowa, N.J; 2005:41-80.

37.

Schwartz L, Major EO: Neural progenitors and HIV-1-associated central nervous system disease in adults and children. Curr HIV Res 2006, 4: 319-327. 10.2174/157016206777709438CrossRefPubMed

38.

Smits HA, Rijsmus A, van Loon JH, Wat JW, Verhoef J, Boven LA, Nottet HS: Amyloid-beta-induced chemokine production in primary human macrophages and astrocytes. J Neuroimmunol 2002, 127: 160-168. 10.1016/S0165-5728(02)00112-1CrossRefPubMed

39.

Bakhiet M, Mousa A, Seiger A, Andersson J: Constitutive and inflammatory induction of alpha and beta chemokines in human first trimester forebrain astrocytes and neurons. Mol Immunol 2002, 38: 921-929. 10.1016/S0161-5890(02)00019-6CrossRefPubMed

40.

Bajetto A, Bonavia R, Barbero S, Florio T, Schettini G: Chemokines and their receptors in the central nervous system. Front Neuroendocrinol 2001, 22: 147-184. 10.1006/frne.2001.0214CrossRefPubMed

41.

Belmadani A, Tran PB, Ren D, Miller RJ: Chemokines regulate the migration of neural progenitors to sites of neuroinflammation. J Neurosci 2006, 26: 3182-3191. 10.1523/JNEUROSCI.0156-06.2006PubMedCentralCrossRefPubMed

Title: Directed migration of human neural progenitor cells to interleukin-1β is promoted by chemokines stromal cell-derived factor-1 and monocyte chemotactic factor-1 in mouse brains
Authors: Yumei Wu
Qiang Chen
Hui Peng
Huanyu Dou
You Zhou
Yunlong Huang
Jialin C Zheng
Publication date: 01-12-2012
Publisher: BioMed Central
Published in: Translational Neurodegeneration / Issue 1/2012
Electronic ISSN: 2047-9158
DOI: https://doi.org/10.1186/2047-9158-1-15

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Directed migration of human neural progenitor cells to interleukin-1β is promoted by chemokines stromal cell-derived factor-1 and monocyte chemotactic factor-1 in mouse brains

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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